101F90051
Criteria For Choosing Indicator Species for
Ecological Risk Assessments at Superfund Sites
Prepared for:
Dr. Andrew Podowski
Waste Management Division
USEPA Region V
Prepared by:
Thomas H. Angus
NNEMS Graduate Student Intern
Environmental Science and Engineering Department
University of North Carolina
Chapel Hill, North Carolina
5 L.brary -- ,. ,„ floor
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DISCLAIMER
This report was furnished to the U.S. Environmental Protection
Agency by the student identified on the cover page, under a National
Network for Environmental Management Studies fellowship.
The contents are essentially as received from the author. The
opinions, findings, and conclusions expressed are those of the author
and not necessarily those of the U.S. Environmental Protection
Agency. Mention, if any, of company, process, or product names is
not to be considered as an endorsement by the U.S. Environmental
Protection Agency.
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Table of Contents
page
Ob j ective .. 1
The Indicator Species Concept
Definition 2
History of Concept 3
Chemical Stress and Indicator Species 4
Advantages 6
Disadvantages 7
Conclusion 8
Terrestrial Organisms
Aquatic vs Terrestrial Organisms 10
Introduction 11
Plants 13
Invertebrates 14
Vertebrates 14
Aquatic Organisms
Introduction 16
Periphton 18
Phytoplankton 19
Macroinvertebrates 19
Fish 21
Criteria for Choosing Indicator Species
Introduction 23
Confounding Factors 24
Criteria Summarized 28
Wide Distribution 30
Ecosystem Integration 30
Residency Status 31
Available Information and Data 31
Species Sensitivity 32
Minimize Informational overlap 34
Historical Information 34
Easily and Accurately Collected/Monitored 35
Temporal Contiuum of Reproducing Stocks 36
Suitable for Laboratory Experiments 36
Social Value 37
Size 37
Exposure to Contaminants 38
Life Stage 40
Critical Species 40
Low Redundancy and Immigration 42
High Reliablility/ Specificity of Response....42
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Objective
The purpose of this paper is to develop criteria for
choosing indicator species for ecological risk assessments
at Superfund sites. The paper begins with an introduction of
the indicator species concept and a brief review of the use
of indicator species in terrestrial and aquatic
environments. Criteria for choosing species are then
outlined and explained.
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The Indicator Species Concept
indicator Species Definition
An indicator is "an organism or ecological community so
strictly associated with particular environmental conditions
that its presence is indicative of the existence of these
conditions" (Morrison 1986). The presence or absence of
indicator species is commonly used to assess adverse impacts
on ecological communities. Indicator species are organisms
that are selectively adapted to certain pollution
conditions, either heavily polluted or clean. The term
"indicator species" has also been applied to organisms that
bioaccumulate toxic substances present in trace amounts in
the environment. This second definition, however, is not in
keeping with the original application of the term and
bioaccumulating species are more properly referred to as
"chemical monitor species" (Connell and Miller 1984).
Indicator species can be divided into two types, class I
and class II (Ryder and Edwards, 1985):
Class I Indicator Species. Class I indicator species are
specialized organisms that have narrow tolerances for most
environmental properties. These are stenoecious organisms
that have evolved to be specially adapted to pristine
conditions. Selected attributes of type I indicator
organisms may serve as early warning indicators of
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perturbations such as chemical stress from a hazardous waste
site. The attribute most often chosen is population decline.
Class I organisms tend to signal earlier environmental
degradation than class II organisms. Class II organisms fill
the niches which are emptied by the decline of class I
organisms.
Class II Indicator Species. Class II indicator species are
less specialized organisms that have relatively broad
tolerances for many environmental properties. These
organisms are euryecious and are outcompeted by stenoecious
organisms in the environments to which the latter are
specially adapted. Type II organisms therefore tend to be
present in low numbers in healthy ecosystems. However,
tolerant organisms are better adapted to the degraded
conditions of a stressed system. Thus an increase in the
populations of class II organisms can signal the degradation
of environmental conditions.
History of the Indicator Species Concept
In 1908 Kolwitz and Marsson proposed the "saprobien"
spectrum, which used continuity composition to assess the
effects of organic pollution on aquatic ecosystems. They
developed lists of organisms associated with various zones
of pollution, differentiated according to the degree of
organic matter in the system. These zones ranged from the
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polysaprobic (large amount of decomposable organic matter
and a low dissolved oxygen concentration) through the alpha
and beta zones of recovery, to a clean water oligosaprobic
zone. Zones were the "centers for optimum growth and
development" for the organisms associated with them. An
investigator then collects and identifies the organisms at a
location, and compares them with a list to determine the
level of organic pollution.
This system was then refined by various scientists in
Europe (Thomas 1975, Sladecek 1965). However, this system
relied on species sensitivity to dissolved oxygen content in
water and did not take into account the toxic pollutants
present today. The importance of the saprobian system is its
introduction of the indicator species concept.
Chemical Stress and Indicator Species
For areas such as hazardous waste sites the emphasis on
indicator species needs to be shifted from dissolved oxygen
sensitivity to toxic substance sensitivity. For Toxicants,
there is a large difference in susceptibility between
species (Slooff 1983). Differences in susceptibility of
species occupying key places in the food web may have
drastic consequences for the structure and function of an
ecosystem. Changes in chemical conditions can result in the
appearance of characteristic taxa, although these often
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represent large population increases in previously
inconspicuous taxa rather than colonization (Ford, 1988).
Changes in species composition may be so imperceptible as
the elimination of only one of the most sensitive species.
This species may be of minor ecological importance or
concern. However, if this is a major species such as a fish
or an important fish-food organism, this may give rise to a
great deal of concern (Hawkes 1982). More intense chemical
stress may affect large numbers of organisms in an
ecological community. Chemical stress can result in
individual species replacements when stressor-tolerant
species replace stressor-sensitive ones. Other affects on
species are more common than straight-forward mortality.
Sensitive species losses may not be directly attributable to
the chemical stress, but the stress may leave the organism
open to other threats such as fungal or insect attacks, or
failure in pollination due to deleterious effects on honey
bees or other sensitive animals (Borman, 1983). Areas such
as resource gathering and reproduction may also be affected.
Shifts in dominance may occur at different trophic levels.
Increased levels or duration of chemical stress not only
cause the disappearance of type I indicator species, but
lead to increases in the numbers of Type II indicator
species. Blooms of opportunistic species normally controlled
by competition or predation appear. Blooms create new food
supplies for decomposer species, and can lead to a temporary
increase in decomposer species (Ford 1988).
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The ecosystem response to a stressor depends on the point
of attack of the stressor on the system as well as other
properties of the system. A proper ecological assessment
based on indicator species needs a thorough knowledge of the
relationships between the type of the stress and the
response of the system. When dealing with disturbance caused
by toxic chemicals, knowledge is insufficient and
environmental assessment is seriously hampered (Sloof 1983) .
Advantages of the Indicator Species Approach.
The Indicator species approach has many advantages:
-Indicator species are a relatively easy, inexpensive and
accurate ecological measure if chosen correctly.
-Indicator species serve as continuous monitors of
pollution at a hazardous waste site, integrating
fluctuations in exposure over time.Indicator species can
also demonstrate when conditions are returning to normal.
-Indicator species are a direct measure of the effects on
the ecology of an area. There is no need to extrapolate from
laboratory tests.
-Effects on indicator species populations are easily
understood by managers, regulators, and the general public.
-Indicator species are useful in identifying specific
species at risk (EPA 1989b).
Karr (1986) writes that indicator species are a useful
measure of the biotic integrity of an area. He defines
biotic integrity as the ability to support and maintain "a
balanced, integrated, adaptive community of organisms having
a species compostion, diversity, and functional organization
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comparable to that of the natural habitat of the region."
Systems with biotic integrity can withstand or rapidly
recover from natural and human induced perturbations.
Systems without biotic integrity are often already degraded
and when further perturbed are likely to change rapidly to
even more degraded states. Karr uses the "index of biotic
integrity" he developed as applied to fish to determine
perturbations to aquatic ecosystems.
Disadvantages of the Indicator Species Approach.
In recent years there has been a growing dissatisfaction
among scientists with the use of indicator species (Cairns
1986, Ford 1988). Biologists have been pushing for a whole
ecosystem approach. Whole ecosystem studies are a great deal
more costly and time consuming. The arguments against
indicator species are outlined below:
No single taxa have emerged as the accepted standard among
all biologists (Cairns 1974).
Anthropogenic chemicals may cause stress to exposed
organisms that leads to gradual degradation of cumulative
changes rather than immediate loss of organisms (Weinstein
1988).
-Absence of indicator species may be due to factors other
than anthropogenic chemicals, such as competition,
predation, lack of colonization potential, inadequate
sampling intensity, and chance. Presence of indicator
species can also be misleading as they may be present in low
numbers in undisturbed systems.
-The signal of the response to chemical stress may not be
discernable from natural variations in species populations
(Kelly et al 1988).
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-If an ecosystem is subject -to more than one chemical
stress, as is often the case at hazardous waste sites, the
indicator species concept may be difficult to apply as
different species respond differently to various sets of
stressors (Ford 1988). A variety of toxic chemicals will
result in a non-specific decrease of species richness and
population size (Sloof 1983).
-Although many indicator species are common, many other
are uncommon or rare in a community, and their presence and
especially their absence may be difficult to demonstrate.
Under ideal circumstances, a biological monitoring program
would include many taxa on different trophic levels, but
time and money do not usually allow this (Cairns 1974).
Conclusion
Whether or not animals are strongly associated with
specific environmental conditions and share these
associations with others is currently under debate (Mannan
et al 1984). The use of indicator species has not been
critically evaluated. The circumstances under which plants
or animals may provide insight into environmental
degradation, or the specific organisms that may best serve
as the the indicators of degradation have not been well
defined (Morrison 1986). The following two sections of this
paper will briefly outline what information is available for
plant and animal indicator species in aquatic and
terrestrial ecosystem. The value of the indicator species
approach is low in the absence of other supporting data. But
careful choice of indicator species applied to well defined
problems may be useful in detecting regional and site-
specific contamination. The value of the indicator species
approach is enhanced if groups of indicator species are
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used. It is particularly useful if they are chosen from
different guilds or trophic levels (Kelly et al 1988). If
groups of indicator species all begin to show changes the
likelihood that the changes are caused by factors other than
chemical stress is greatly reduced.
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Terrestrial Organisms
Aquatic Verses Terrestrial Organisms
Indicator species have been much more extensively used
for aquatic ecosystems than they have for terrestrial
ecosystems. In forest ecosystems the dominant producers are
trees. Trees reproduce and grow slowly. If they are killed
it may be years before they are replaced. A gradual movement
from pollution sensitive to pollution resistant species
occurs in both terrestrial and aquatic ecosystems. This
trend is much slower in terrestrial ecosystems. The turnover
time for terrestrial ecosystems may be years or centuries
instead of days. Therefore changes are not detectable nearly
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as early in terrestrial ecosystems as they are in aquatic
ecosystems. However, it will also take a lot longer for a
terrestrial ecosystem to recover so detection of terrestrial
perturbation may be even more important in terrestrial
ecosysytems (Schindler, 1987). Terrestrial soils tend to
concentrate pollutants, thus exposing the primary producers
to toxic chemicals. In aquatic ecosystems the key primary
producers are phytoplankton. They are exposed to toxic
pollutants only if those pollutants are water soluble.
Introduction
A chronic xenobiotic chemical is stress a terrestrial
ecosystem is likely to have been previously exposed to. Many
organisms are likely to be sensitive to the chemical, as
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evolution would not have had time to eliminate sensitive
species. Various organisms in a terrestrial ecosystem are
differentially susceptible to toxic compounds.
Microorganisms capable of detoxifying and breaking down
xenobiotics are not likely to have developed significant
population sizes, if they exist at all. Studies by Sheehan
and Winner (1984) found that pollutants tend to affect
species compostion and succession by replacing advanced
communities with species of earlier serai stages (see also
Woodwell 1983, Odum 1985).
Plants
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Early use of indicator species primarily took the form of
plants used to identify habitat types. Dominant autotrophs
determine ecosystem structure to a large extent, so much has
been done to study changes to these organisms (Weistein
1988). Plants have been used in studies of both soil and air
pollution (Jones and Heck 1981, Martin and Coughtrey 1982,
Dewit 1983, Eijsackers 1983, Ernst 1983). Certain plants
have been shown to be abundant in metal contaminated soils
(Hutton 1984). Ten Houten (1983) found that plants are
generally more suitable for air pollution studies than
animals because they "ask less attention and react
frequently with characteristic symptoms to low
concentrations of specific air pollutants". Air pollution
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from volatile organics is an important consideration when
determining ecological damage at Superfund sites.
Plants have several advantages and disadvantages as
indicator species:
Advantages;
Sedentary.
Easy to identify and usually do not need to be collected.
Ubiquitous occurrence.
Low trophic level organisms.
Disadvantages:
There is not a great deal of datam plant sensitivity to
toxic chemicals. The focus has been on animal species.
Are not useful for hydrophobic bioaccumulating compounds.
May react less rapidly than animals.
Plants may take up chemicals with low log P values
through their roots. They can't transport significant
amounts of compounds with high molecular weights or high log
P values. Plants may become contaminated by soil or water,
or by the volatilization of chemicals at a site.
Patton (1984) claims that plants are the best indicators
of environmental change since they are directly affected by
environmental factors. Animals are not only dependent upon
plants, but are also influenced by environmental factors.
Plants are non-mobile, easy to count, and indicate change
with a high degree of certainty. Perrenial plants are the
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best indicators because repeated measurements can be made at
the same location.
Invertebrates
Terrestrial invertebrates have been used to some extent, but
not to the overwhelming extent they have been in aquatic
environments. Rosenburg (1986) reviews the use of
terrestrial insects in monitoring studies. Soil is the major
terrestrial sink for pollutants, so invertebrates are often
heavily exposed to contaminants. Invertebrates have many
advantages and disadvantages implicit in their use:
Advantages:
small organisms with rapid turnover rates in which effects
are likely to occur earlier.
High species diversity
Ubiquitous occurrence
Often abundant and easily sampled
Ecological and Economic Importance -decomposition of
organic matter, provision of food for fish and wildlife,
purification of groundwater.
Disadvantagesi
Small and cryptic in coloration and behavior -not as
easily observed as birds or mammals.
Identification and analysis of samples is time consuming
and expensive.
Species level taxonomic data is often lacking (Whitby and
Hutchinson 1974).
Variable soil types need to be characterized in order to
choose species.
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Decomposer organisms in the litter layer appear to be
relatively sensitive to metals because of their intimate
exposure to them (.Hutton 1984). For example, earthworms are
efficient accumulators of both metals and organochlorine
compounds, and give a measure of the relative amounts
entering the foodchain. The species Allobophora Calliginosa
has been shown to be especially sensitive in studies with
copper, cadmium, zinc, fly ash, and sewage sludge
(Eijsackers 1983). Earthworms burrow through the upper soil
layers (20-100 cm) thus integrating the toxic components of
these different layers. Organisms that are soil ingestors
like earthworms are particularly useful because they are
highly exposed to pollutants in soil.
Vertebrates
Vertebrates have not been used extensively to monitor for
environmental contaminants.
Advantages;
High ecological, economic, and social value
Conspicuous and easily observed
Extensive taxonomic, life history and chemical sensitivity
information.
Upper trophic level organisms which are especially
susceptible to bioaccumulating compounds.
Disadvantages;
Effects of environmental contaminants occur relatively
late when compared with smaller organisms with higher
turnover rates.
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Populations tend to be small, and absence may be due to
demographics or inadequate sampling.
Birds are the most extensively used vertebrate indicator
species (Roberts 1985, Block et al 1986, Block et al 1987).
Birds are often the most conspicuous organisms within
ecosystems (Morrison 1986). They also appear to be more
sensitive to environmental contaminants than other
vertebrates (Stickel 1975, Grue et al 1983). Rats, mice, and
rabbits are other vertebrates that have frequently been
favored as indicator species. This is not because of their
inherent sensitivity but because of the wealth of laboratory
data available which aids in correlating population
decreases with the presence of environmental contaminants.
Sylvia Talmage (1989) assessed the merits of using small
mammals as monitors for environmental contaminants. There
was a correlation between the amount of contaminants in the
soil and in small mammals. The concentrations of
contaminants generally increases with higher trophic level
organisms.
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Aquatic organisms
introduction
The use of indicator species is more prevalent in aquatic
it is in terrestrial ecosystems (Phillips 1978, Angermeier
and Karr 1986, Peterson 1986, Courtemanch and Davies 1987,
Klerks and Levington 1989). This is because aquatic
ecosystems have been the traditional receptors for municipal
and industrial waste. Most of the work that has been done
with indicator species has been in regards to municipal
sewage. However organisms respond very differently to sewage
than they do to toxic chemicals. High sewage concentrations
favor organisms that can survive in environments with a low
dissolved oxygen content. Toxicity is the main concern with
chemical compounds at hazardous waste sites.
In contrast to the relatively slow reactions of
terrestrial ecosystems, aquatic systems are very dynamic.
Heterogeneity is a particularly severe problem in aquatic
ecosystems. It is often difficult or impossible to measure
the variability of a system. This is particularly important
in weighing the presence or absence of a species. Aquatic
community structure is often cryptic, and stochiastic
factors are important in determining ecosystem structure and
dynamics. Even normal seasonal successional changes are more
variable than in terrestrial systems (Ford 1988). The large
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numbers of chemicals and ecosystem types make the two very
difficult to match in terms of expected effects and changes.
Large lakes are.temporally stable physiochemical
environments that can also be surprisingly patchy arid
changing in terms of community structure. Stratification and
mixing lead to cryptic differences in species abundance and
ecosystem structure. The sampling intensity necessary to
account for ecosystem variability can be great.
Rivers and streams are at the other extreme from lake
ecosystems. Lotic systems are temporally variable and a
longer monitoring period may be necessary to characterize
lotic systems than non-moving systems. This can be overcome
however by monitoring a section of stream upstream from the
site as well as a section that is being affected by the site
(Stauffer and Hocutt 1980). This allows for comparison
between the two sections. Care must be taken that the
ecosystem types of the two sections and extraneous factors
are not significantly different.
For aquatic systems it is necessary to determine
ecosystem properties such as substrate, flow, and
temperature. In most aquatic ecosystems the sensitive
indicators of stress include changes in sensitive short-
lived species and changes in community structure resulting
from the elimination of keystone predators (Schindler 1987).
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Periphyton
Periphyton are complex assemblages comprised of
autotrophs (algae), .and heterotrophs (fungi, bacteria, or
protozoa) attached to substrates in lotic environments. They
are sometimes are sensitive indicators of environmental
contaminants in lotic ecosystems (Lewis et al 1986). "Non-
diatom species predominate in in polluted and recovering
areas. Studies have shown declining species diversity and
species richness which demonstrate a loss of sensitive
species with a concurrent increase of more resistant species
(Crossey and Lapoint 1988, Steinman and Mclntire 1990).
Advantages t
Small and rapidly reproducing, are among the first
organisms affected
Ubiquitous occurrence
Easy to collect
Ecological importance - food sorce for higher trophic
level organisms
Disadvantages t
Relatively little information available on species
sensitivity
Difficult to identify
Little data available
t
Phytoplankton
Phytoplankton have not been used extensively as indicators
of chemical contaminants (Shubert 1984). Changes in
Phytoplankton species composition are thought to be among
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the most sensitive indicators of ecosystem stress, but
collection and identification problems have kept
phytoplankton from being used (Schindler 1987).
Advantages:
Among the first organisms to show changes in species
dominant because they are small, rapidly reproducing, and
disperse widely.
Are sensitive to a large number of compounds:
organochlorines such as DDT and PCBs, and trace elements
such as copper, zinc and mercury,
Disadvantages s
Difficult to obtain sort samples - species identification.
Rapid species succession can cause acute responses to be
masked -little time integration.
Have not been used extensively -data are lacking.
Macroinvertebrates
Aquatic macroinvertebrates are the most commonly used
organisms for the ecological assessment of environmental
contaminants (Resh and Unzicker 1975). Many studies have
been performed using aquatic macroinvertebrates (Lenat et al
1983, Schaeffer et al 1985, Hilsenhoff 1988). Because
pollutants are generally more concentrated in sediments than
in the water column, benthic macroinvertebrates are exposed
to greater concentrations of pollutants than pelagic or
planktonic organisms. Thus benthic organisms are the
macroinvertebrates most commonly chosen (Morse 1983). Many
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benthic organisms are among the most sensitive higher
aquatic species, even to pollutants such as acids which are
not concetrated in.sediments (Schindler 1987).
Aquatic macroinvertebrates exhibit a steady, predictable
response to heavy metals and other compounds. In streams
extensively polluted with heavy metals, all species except
for tubificid worms and chironomids were virtually
eliminated (Winner et al 1980). Mayflies were found to occur
only at he least polluted areas while heavily polluted areas
were dominated by midges. Chironomids comprise a very small
fraction of the fauna in unpolluted streams in North
America, but comprise 40-75% of the fauna in streams
contaminated with heavy metals. Caddis flies wer eliminated
at the most seriously polluted parts of streams but were co-
dominant with chironids in moderately polluted parts of
streams (Sheehan and Winner 1984).
Advantages;
Large enough for easy collection
Are not mobile enough to leave an area of pollution
rapidly
Can be studied in labs easily
Exist in all aquatic environments
Life cycle is short enough that short term effects of
pollutants will not be overcome until the following
generation.
Communities heterogeneous, several phyla usually
represented, therefore chances are high that some groups
will respond to environmental contaminants (Hellawell 1986).
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Disadvantages:
Quantitative samples may be difficult to obtain.
Species that drift may be found in areas where they
normally don't occur.
Sorting and identifying species may be time consuming and
expensive (Berkman 1986).
Species level taxonomic and life stage information may be
lacking.
Chemical sensitivity data are often lacking.
Under certain circumstances benthic macroinvertebrates may
not be affected by pollution discharges of short duration
that may affect organisms in the water column (Hawkes 1982).
Fish
Fish are commonly used as bioassay organisms, but they
have rarely been used in comprehensive monitoring studies.
Fish are becoming more popular as indicator species. Many
scientists have decided that the advantages of fish as a
monitoring species outweigh the disadvantages (Karr 1981,
Hocutt 1981).
When there is a large number of non-migratory species of
various ages and normal growth rates, than pollution has not
likely occurred recently. The presence of fish is more
useful than their absence because of their motility
(Goodnight 1973). Karr (1986) has found both the proportion
of omnivores and presence of top carnivores to be important
in determining pollution levels. Omnivores constitute less
than 20% of the fish in an unpolluted ecosystem. A
proportion of omnivores of greater than 45% indicates gross
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pollution. Presence of top carnivores indicates a relatively
healthy and trophically diverse ecosystem.
Advantages;
Commonly used as a bioassay organism -there is a great
deal of data on chemical sensitivity.
Economic, recreational, and aesthetic value.
Identification is relatively easy compared to smaller
organisms.
Much information available on the environmental
requirements and life histories of fish.
Fish are "integrators" of lower trophic levels (Hendricks
et al 1980)
Long lived -temporal integration
Species occupy many trophic levels
Most species reproduce once a year leading to stable
populations in the summer when most sampling occurs
Contain upper trophic level species which will
bioaccumulate hydrophic compounds.
Disadvantages:
Mobile and can move away from contaminated areas.
Numbers are fewer than with smaller organisms, leading to
a greater chance of sampling error being responsible for
presence or absence. It may also cause sampling to affect
the success of a species at the site.
Quantitative samples are difficult to obtain.
Have rarely been used -are not tried and tested.
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Criteria For Choosing Indicator Species
Introduction
The selection of a suitable organism is one of the first
and most important tasks in environmental risk assessments
once the decision to use indicator species has been made. An
incorrect decision at this stage may render the ecological
assessment useless. The species choice will be influenced by
the needs of the survey as well as by site-specific
characterisitics of the hazardous waste site. The choice of
the site should reflect the aquatic and terrestrial
resources at risk.
Two different branches of the federal government have
already developed criteria for choosing indicator species.
The United States Fish and Wildlife Service (USFWS
1980a,b,c) and the United States Forest Service (Code of
Federal Regulations 1985) have developed criteria for
choosing indicator species. The United States Fish and
Wildlife criteria are as follows:
Ecological Criteria:
Sensitivity to specific environmental factors.
Keystone species (exert a major influence on the
community).
Single species representative of a guild.
Socioeconomic Criteria:
High public interest value.
High socioeconomic value.
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The United States Forest Service has developed criteria for
choosing "management indicator species" :
Recovery species - those identified by state or local
government as threatened, endangered, or rare.
Featured species - those of high socioeconomic value.
Sensitive species - those identified by regional foresters
as having habitat requirements particularly sensitive to
management activities.
ecological indicators - Those used to monitor the state of
environmental factors, population trends of other species,
or habitat conditions.
Specific goals, objectives, and standards for management
indicator species appear in each National Forest Plan that
the United States Forest Service is required to develop
(Code of Federal Regulations, 1985). These criteria were
developed to monitor the impact of management activities on
federal land rather than to monitor for ecological
contamination with toxic chemicals.
Confounding Factors
Introduction
Choosing indicator species is a difficult task. A number
of factors confound the choice of an indicator species.
Even well defined ecosystem types have a variety of
trophic structures and redundancy characteristics. Key
species and processes may also vary (Ford 1988). Thus
different species are important in different ecosystems and
these species can vary widely in their sensitivity to a
number of chemical contaminants present at a hazardous waste
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site. Several floral and faunal groups should ideally be
incorporated into an integrated ecological assessment.
(Roberts 1985). Practical consideration such as time and
money often require that a single species be used. This
makes the choice of a proper species crucial.
It is difficult to choose between monitoring for the
presence of a tolerant species or the absence of an
intolerant one to determine environmental degradation
through chemical contamination. Sensitive species must
decline in abundance before the less competitive tolerant
species can increase in abundance. Thus sensitive species
are an earlier indicator of environmental degradation.
However most scientists use the presence of a tolerant
species in determining chemical contamination. Organisms
have a wide range of tolerance to pollution conditions.
Therefore an observed absence of non-tolerant species is of
greater significance than the presence of tolerant species
(Lenat et al 1983).
Cairns (1974) however, has a different point of view. He
notes that the presence of a species indicates that certain
minimal environmental conditions have been met. The absence
of a species is the more risky choice because of possible
confounding factors:
The environmental conditions are unsuitable.
The species has not had a chance to colonize the area but
would do so if introduced.
Another species has assumed the functional niche.
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The presence of an indicator species is more useful, but the
absence of species can be equally useful if a group of
species with similar needs and sensitivities are absent.
Species present/absent due to factors other than
tolerance/intolerance. Species may be present or absent due
to a number of factors. Species are affected by many factors
such as fire or drought, extreme weather conditions, or
unknown conditions in areas such as migration routes or
wintering grounds. Natural variability and successional
changes within the ecosystem may cause changes in species
compostion over time.
Competition, predation, and disease are factors which can
lead to the presence or absence of a species. These three
factors, however, are in turn affected by environmental
contaminants. Chronic exposure to toxic chemicals can lead
to weakness or behavioral abnormalities in organisms. This
can cause a species to lose its ability to compete with
other organisms or escape a predator. A predator may be
affected by a chemical compound and be killed or unable to
catch prey as successfully which could lead to a shift in
the competitive balance of lower trophic levels. Toxic
chemicals may also may a species more susceptible to
disease. Thus competition, predation, and disease may cause
the presence or absence of a species, and in turn be
affected by the introduction of toxic .chemicals. It is
important to try to separate out the influence of these
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factors while at the same time evaluating the importance of
toxic chemicals in contributions of these factors to the
presence or absence of species.
Differences in comparing one site to another. An
indicator that is appropriate in one area may not be
appropriate in another area. Geographically separated areas
may appear similar but have subtle differences. These
differences can occur in the dominant or subdominant species
of plants and animals, or in the species performing vital
ecosystem functions. There may be different natural
disturbances in the area, and habitat and resource
patchiness. An organism which is found in one ecosystem may
not have been introduced to a second ecosystem.
Ambiguous, ill-defined, and confounded criteria. Criteria
for choosing indicator species need to be unambiguously and
explicitly defined. In the practice of choosing indicator
species, criteria are often confounded (Landres et al 1988).
A species used to fill one criterion should not be used to
fulfill a second criterion unless it explicitly meets the
needs of the second criterion. A species with a high
socioeconomic value will sometimes be used to fullfill an
ecological criterion. This is not appropriate unless it
fulfills both criteria. Species should not be used for
multiple roles without research verifying that the species
is appropriate for both criteria. The reasons for having
each criterion should be explicitly stated.
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Sources of subjectivity. All of the sources of
subjectivity in selecting indicator species must be
identified and defined. These sources will vary depending on
the attributes of the site and the ecosystem and species
types found on the site. All assessments and technical
decisions inherently contain value judgments which should be
discussed so that the merits and difficulties of each may
determined.
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Criteria. Summarized
1. Wide Distribution
2. Ecosystem Integration
3. Residency Status
4. Available Information and Data
5. Species Sensitivity
6. Minimize Informational Overlap
7. Historical Information
8. Easily Collected and Monitored
9. Temporal Continuum of Reproducing Stocks
10. Suitable for Lab Experiments
11. Social Value
12. Size: Small - Short Term, Large - Long Term
13. Exposure to Environmental Contaminants
14. Life Stage
15. Critical Species
16. Low Redundancy and Immigration
17. High Reliability and Specificity of Response
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Criteria
When using the criteria, candidate organisms may be
arranged by taxonomic class in order to make them easier to
compare. An ideal organism would fulfill all of the
following criteria. However, the following criteria are
extensive, and it may be difficult or impossible to find one
organism that fulfills all the criteria. However, several
organisms taken together should be able to fulfill the
criteria and provide important information for an ecological
assessment.
Wide Distribution. Potential indicator organisms should be
widely distributed in the area. This will allow for
comparison with other sites in the area. Candidate species
should be screened for orgnanisms whose geographic range
does not include the area of the hazardous waste site or who
require special habitat features not found at the site (Fry
et al 1986). The species should also be abundant enough to
be easily found. This minimizes the risk that a species will
be misclassified as present or absent. It also minimizes the
risk that the populations will be affected by any samples
taken.
Ecosystem Integration. The"organism chosen should display
at least a moderate level of ecosystem integration. It
should interact with many other natural and human components
of the community. An organism which interacts with many
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other parts of the community will generally have more
importance to the system and therefore more relevance in
measuring the degradation of the ecosystem.
Residency Status. When monitoring for the absence of an
intolerant indicator species it is important for the
organism to be indigenous and a structurally stable
component of the ecosystem. Such an organism will be adapted
to relatively unperturbed conditions (only for abscence).
Indicator species should be permanent residents of the site.
Migrating species are affected by many offsite factors.
However, migrating species are often included for other
reasons such as socioeconomic factors (Landres et al 1988).
Available Information and Data. The biology of the
organism should be known in detail. This should include
behavioral response, life history, and interactions with
other species. This will aid in the evaluation of an
organism's response. The organism's responses to a wide
range of environmental conditions should also be known
(Lenat et al 1983). This will help ensure that environmental
factors other than chemical sensitivity will not be
responsible for an the presence of a tolerant species or the
absence of an intolerant species. Niche requirements and
habitat characteristics should be known and supported by
adequate scientific information. This will allow the
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investigator to determine that the organism's absence is not
due to unmet niche needs or unsuitable habitat at the site.
Using quantity of information as a selection criteria
reduces time and costs in terms of additional research that
may have to be done on the organism (Landres et al 1988).
This often has the drawback of reducing the relevance of the
organism for an ecological assessment. Little information
may exist for a relatively sensitive indicator while a great
deal of information exists for a sensitive one. The less
sensitive indicator may be chosen while the more sensitive
species is the better indicator of environmental conditions.
This criterion must be used carefully and in conjunction
with the relative senstivity of the organism.
Species Sensitivity. Indicator Species should be chosen
based on thier sensitivity to the specific environmental
contaminants which must be monitored. Sensitivity to toxic
chemicals is a crucial element in choosing an indicator
species. Those species that are most sensitive to
contaminats potentially make the best indicator species
(Szaro and Balda 1983). Organisms differ in their relative
abilities to take in, accumulate, metabolize, distribute ,
and eliminate contaiminants. Together, these attributes
result in often extreme differences in species relative
sensitivities to environmental contaminants. However, these
attributes can differ dramatically from chemical to
chemical. Consequently, exposure to two different chemicals
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can produce two markedly different responses. It is
important to determine the contaminants of concern at a site
and to match these.contaminants with species that are
relatively sensitive or insensitive to them.
The organism chosen should be at one end of the range,
either extremely sensitive or extremely insensitive to toxic
chemicals. It may also be useful to choose species that by
themselves or in conjunction with one another will exhbit a
graded response to a range of increasing levels of
environmental contamination. For example, Sheehan and Winner
(1984) that in streams polluted with heavy metals, mayflies
were a significant part of the insect community only at the
unpolluted sites. Caddis flies were co-dominant with
chironomids at moderately polluted sites while they were
eliminated at the most grossly polluted sites. Chironomids
were most abundant at the most grossly polluted sites. Thus
the level of contamination could be roughly determined by
the relative proportions of the three types of insects.
Sensitivity to the contaminants of concern should have a
direct cause and effect relationship, rather than a
correlation. Otherwise the effect of contaminants on
populations may not be separable from other regulating
factors such as competition, predation, and disease (Landres
et al 1988).
It is also important for sensitive organisms to have a
relatively rapid response to environmental contaminants
(Kelly and Harwell 1988). Where possible, it should be among
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the first species to be affected by a pollutant. This often
means a species at a low trophic level. The length of time
it takes for a species to be affected by toxic chemicals
depends on both species sensitivity and exposure.
Paleoecological studies are becoming more important in
determining species sensitive to pollutants (Schindler 1987,
Ford 1988). They offer the opportunity to examine changes in
community structure at sites that have already experienced
chemical stress.
Minimize Informational overlap. Species should be chosen
in such a way that they complement the other information
used in the ecological assessment (Ryder and Edwards 1985).
Different indicators should reflect different areas of
concern. Informational overlap should be minimized insofar
as is possible. This will prevent redundancy in information
obtained and provide for the most efficient use of the
monitoring resources utilized. It is also helpful if
indicator species are chosen from different guilds are
trophic levels, to monitor as much of the ecosystem as
possible (Kelly et al 1988).
Historical Information. Species should be chosen based on
the information available on the species' history in the
ecosystem. Information is necessary on the species' natural
baseline condition and its range of variation in the
ecosytem. The species should have one or more historic data
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35
series for comparison with the present. The data should show
quantifiable evidence for the relative abundance or scarcity
of an indicator species during a period of relatively little
contamination. Information on the organism at the site can
be supplemented by reviewing information on previous work
performed on the organism in similar ecosystems. This
information will help confirm that the population decline or
increase of a species is due to chemical contaminants.
An alternative to this is to have a similar site for
comparison with the contaminated site, but if this is done
care must be taken to account for confounding factors i.e.
differences in food web structure, nutrient abundance,
disease incidence, habitat type.
Easily and Accurately Collected and Monitored. It is
important to use a species that can be collected and
measured easily to determine the standing stock in terms of
numbers and biomass. This will decrease the time and cost
expenditures of the evironmental assessment and increase the
accuracy of the results (Berkman 1986). In order for a
species to be easily collected and monitored it must have a
fairly high population density. Organisms with a low
population density lead to sampling problems which may make
an accurate assessment impossible despite the organism being
a good indicator in other ways. Long term research is needed
on each indicator species to assess natural variation in
population density no related to environmental contaminants
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36
which may confound results. Population density must be
balanced with species sensitivity however and Zyromska
(1977) and Freckman et al (1980) showed that less abundant
species are relatively sensitive to adverse influences.
Szaro and Balda (1983) said that organisms with the
following three attributes were relatively easy to monitor:
-Conspicuous by sight and sound.
-Easy to recognize in the field without the observer
having to capture the species to identify it.
-Operate during the hours which man is active.
Temporal Continuum of Reproducing Stocks. A temporal
continuum of reproducing stocks serves several purposes .It.
*-»•%
assures that the organism is a permanent part of the
ecosystem which is unlikely to increase or disappear for
other reasons. It also allows for continued monitoring of
successive generations to determine improvment or further
degradation at the site. The organism should be. sufficiently
long lived for the examination of more than one year class
if desired.
Suitable for Laboratory Experiments. The organism should
be suitable for laboratory experiments, especially those
designed to investigate cause and effect relationships. Most
ecological assessments need a combination of field
observation and laboratory experiments of organisms. It is
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37
important to quantify species species sensitivity to an
environmental contaminant in a laboratory setting.
Social Value. It is often helpful to reduce the number of
possible species by looking at those which are important to
humans. The species may be valuable for aesthetic, economic,
educational, scientific, or sporting reasons. These include
threatened and endangered species which appear on current
state and federal lists. Species important for hunting,
fishing, and trapping can be determined using lists obtained
from state departments of fish and game. Species of high
social value are the species for which we have the most
information. They are also the species we are most concerned
with protecting against the deleterious impacts of
environmental contaminants. This criteria has often been the
primary concern when indicator species have been chosen, but
it is not as important as species sensitivity.
Alternatively, organisms which are a vital food source for
an organism of social value may be chosen. The species may
also be one which has a breeding habitat at the site or
which uses the site as part of its migration route. The
problem with migrating species however is they are affected
by many off-site factors.
Size: Short Term - Small Organisms, Long Term - Large
Organisms. The organism should be of a size that makes it
easy to collect or observe. It is important to monitor both
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38
small and large species in order to monitor both short term
and long term changes in ecosystem health. Small organisms
have a shorter lifespan and will react more rapidly to
environmental contaminants. This makes them good indicators
of short-term response or recovery. Larger organisms have a
slower population turnover and tend to take a longer time to
reat to or recover from environmental contaminants. Larger
organisms are better indicators of of long term response or
recovery. Larger organisms are usually easier to observe and
identify. Larger organisms tend to have more stable
populations which makes it easier to detect significant
changes in population size. Large organisms also tend to
range over a larger area and may spend much of their time
off-site, decreasing their exposure to contaminants (Landres
et al 1988).
Exposure to Environmental contaminants. Exposure to
environmental contaminants is an extremely important
consideration when choosing indicator species. It is
important to pick the species which is most exposed to the
contaminated media. The primary uptake routes of the
organism should be considered. Organochlorines tend to be
associated with are associated with particulate matter so a
soil organism or filter feeder should be chosen (Phillips
1980). Synthetic organics such as such as poly-chlorinated
biphenyls and dioxins are soluble in fat and thus species
with a large amount of body fat would be appropriate. Trace
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39
metals such as cadmium exist almost totally in solution so
an organism that exists in the pelagic zone of an aquatic
ecosystem would be appropriate. Landres et al (1988)
cautions that metal pollution in organisms may result from
mobility and transport of the pollutant within the ecosystem
rather than being directly related to pollution
concentration in the environment. Therefore caution and
detailed information is necessary when using indicators of
environmental contaminants.
Water soluble compounds should be investigated for
potential exposure routes to aquatic species. Water soluble
compounds may also move through the aqueous phase of some
soils, increasing the likelihood of exposure to soil
organisms.
Compounds with low water solubility may adsorb to soil
particles and may affect organisms living on or in the
ground. Contaminants adsorbed to soil paticles may also be
carried by erosion to aquatic or other terrestrial sites.
Hydrophobic compounds tend to bioaccumulate and an upper
trophic level organism may be appropriate (Farrington 1988).
Dose is an important element of exposure when looking at
indicator species. A high dose or acute exposure will induce
mortality rapidly. A low dose or chronic exposure will
impair the functioning of some biological process within the
organism (Weinstein and Burk 1988).
The species chosen should preferably be sedentary at most
stages of its life cycle and especially at the life stage of
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40
interest. The organism will be more representative of the
site the site if it does not spend part of its time off-
site. An organism that spends part of its life off-site will
not be as fully exposed to the contaminants at the hazardous
waste site as an organism which is sedentary. Once the
medium which will yield the greatest contaminant exposure
has been chosen a sedentary organism in that medium to
ensure the greatest possible exposure.
Life Stage. When choosing an indicator species it is
important to consider the life stage of interest. A species
may have a life stage that is particularly vulnerable to
environmental contaminants. To cause injury, chemical
exposure must occur at a vulnerable location during a
vulnerable period (Weintein and Birk 1988). The life stage
of interest may cover any one of a number of areas:
-Reproductive success as measured by the survival of
gametes, larva, juveniles, or embryos.
-Survival or juveniles or molts.
-Longevity of adults.
-Incidence of disease, including physiological and
behavioral abnormalities (EPA 1989b).
Critical Species. In order to ensure that the ecosystem is
being adversely affected by chemical contaminants, the
indicator organism should be a critical species. A critical
species is an organism that performs a vital ecosystem
function in the cycle of physical and biological processes
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41
in an ecosystem. A critical species helps maintain the cycle
which which provides all organisms in the community with
sufficient energy and nutrients. As a result, a disruption
in these species would result in a disruption of energy and
nutrient pools. Sheehan (1984) notes a buildup of soil
litter at sites contaminated with heavy metals. This was due
to the loss of critical litter decomposing organisms and led
to a loss of energy and nutrients in the ecosystem. Ecosytem
stability and viability depends upon the continued success
of critical species. Ecosystem decline will be signaled by
the decline of these species. Recovery of ecosystems is also
closely linked with the recovery of critical species
(Weinstein and Birk 1988). Critical species also include top
predators which keep populations under control and maintain
species diversity.
When looking at critical species, it is often useful to
look at shifts in the dominant species in an ecosytem. These
shifts tend to be more ecologically damaging (Ford 1988).
The critical species concept applies to tolerant as well
as intolerant species.The relative abundance of species with
short life cycles changes to favor those that can maintain
critical ecosystem functions in the early stages of
ecosystem stress. Such organisms contain valuable indicators
of stress and may serve as an early warning of contaminant
problems (Schindler 1987). The critical species criterion is
sometimes difficult to apply because few critical species
have been identified although research is continuing.
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42
Low Redundancy and Immmigration. The species should occupy
a place in the food web where both redundancy and
immigration are low. These are the species that are most
important to community structure and stability. If few other
species occupy the functional niche of the species and
immigration is unlikely to occur, then adverse effects to
the organism could significantly effect the food web.
High Reliability and Specificity of Response. The organism
should exhibit high reliability and specificity of response
(Landres et al 1988). In order for this to be happen,
several factors must hold true. Natural variability within
the population must be low. There must also be a high
response rate of individuals in the species to the
environmental contaminant in question. Alternatively, the
contribution from each significant source of variation must
be identified. The organism chosen should have a high signal
to noise ratio (Slooff 1983). The response of the species
should be specific to exposure to the contaminant in
question.
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