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GLOBAL AND REGIONAL ECOLOGY | Lead Editor: Carolyn Malmstrom
By: Emily A. Holt (Department of Watershed Sciences, Utah State University) & Scott W.
Miller (Department of Watershed Sciences, Utah State University) © 2011 Nature Education
Citation: Holt, E. A. & Miller, S. W. (2011) Bioindicators: Using Organisms to Measure
Environmental Impacts. Nature Education Knowledge 2(2):8
How do we assess the impacts of human activities on natural ecosystems? What can
the biota tell us about the environment and its response to natural stress?
Introduction
What can the canary in the coal mine tell us? Historically, canaries accompanied coal miners deep underground. Their small lung capacity
and unidirectional lung ventilation system made them more vulnerable to small concentrations of carbon monoxide and methane gas than
their human companions. As late as 1986, the acute sensitivity of these birds served as a biological indicator of unsafe conditions in
underground coal mines in the United Kingdom. Since human health concerns continue to drive the development and application of
bioindicators, the loss of ecosystem services (e.g., clean air, drinking water, plant pollinators) has increasingly focused our attention on the
health of natural ecosystems. All species (or species assemblages) tolerate a limited range of chemical, physical, and biological conditions,
which we can use to evaluate environmental quality. Despite many technological advances, we find ourselves turning to the biota of natural
ecosystems to tell us the story of our world.
What Is a Bioindicator?
Bioindicators include biological processes, species, or communities and are used to assess the quality of the environment and how it
changes over time. Changes in the environment are often attributed to anthropogenic disturbances (e.g., pollution, land use changes) or
natural stressors (e.g., drought, late spring freeze), although anthropogenic stressors form the primary focus of bioindicator research. The
widespread development and application of bioindicators has occurred primarily since the 1960s. Over the years, we have expanded our
repertoire of bioindicators to assist us in studying all types of environments (i.e., aquatic and terrestrial), using all major taxonomic groups.
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However, not all biological processes, species, or communities
can serve as successful bioindicators. Physical, chemical, and
biological factors (e.g., substrate, light, temperature,
competition) vary among environments. Over time, populations
evolve strategies to maximize growth and reproduction (i.e.,
fitness) within a specific range of environmental factors. Outside
an individual's environmental optima, or tolerance range, its
physiology and/or behavior may be negatively affected, reducing
its overall fitness (Figure 1). Reduced fitness can subsequently
disrupt population dynamics and alter the community as a whole
(Figure 2). Bioindicator species effectively indicate the condition
of the environment because of their moderate tolerance to
environmental variability (Figure 1). In contrast, rare species (or
species assemblages) with narrow tolerances are often too
Figure 1: Comparison of environmental tolerances of (a)
sensitive to environmental change, or too infrequently
bioindicators, (b) rare species, and (c) ubiquitous species
encountered, to reflect the general biotic response. Likewise,
Red areas represent portions of an environmental gradient (e.g.,
ubiquitous species (or species assemblages) with very broad
light availability, nitrogen levels) where an individual, species, or
tolerances are less sensitive to environmental changes which
community, has fitness or abundance greater than zero. The
otherwise disturb the rest of the community. The use of
dashed line represents the peak performance along this particular
bioindicators, however, is not just restricted to a single species
environmental gradient, while yellow boxes include the optimum
with a limited environmental tolerance. Entire communities,
range or tolerance. Bioindicators possess a moderate tolerance to
encompassing a broad range of environmental tolerances, can
environmental variability, compared to rare and ubiquitous species.
serve as bioindicators and represent multiple sources of data to
This tolerance affords them sensitivity to indicate environmental
assess environmental condition in a "biotic index" or
change, yet endurance to withstand some variability and reflect the
"multimetric" approach.
general biotic response.
© 2010 Nature Education All rights reserved.
Furthermore, biological processes within an individual can act as
bioindicators. For example, cutthroat trout inhabit coldwater
streams of the western United States. Most individuals have an upper thermal tolerance of 20°–25°C; thus, their temperature sensitivity
can be used as a bioindicator of water temperature. Livestock grazing, burning, and logging are examples of human-related disturbances
that can increase water temperature in these streams and be detected by cutthroat trout at various biological scales (Figure 2). An
immediate response of cutthroat to thermal pollution occurs at the cellular level. Specifically, heat shock protein (hsp) synthesis increases
to protect vital cellular functions from thermal stress. We can quantify hsp levels to measure thermal stress in cutthroat trout and assess
how the environment has been altered. If thermal stress persists, such physiological changes are generally tractable at the individual level
through behavioral changes and subsequent reductions in growth and development. In the most extreme instances, however, large and
persistent thermal alterations can reduce population numbers and even lead to local extinctions, causing compositional shifts to warmwater
fisheries.
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Figure 2: Diagram of the hierarchical levels of an ecosystem that respond to anthropogenic disturbances or natural stress
The white ring of environmental variables includes factors that may be directly altered by disturbance or stress. These alterations
may subsequently affect individual organisms, populations, or the community as a whole. The outermost colored ring represents
individual organisms (cutthroat trout, Pteronarcys Salmonfly, Phaedoactylum diatom), the middle colored ring represents populations
of those organisms, and the innermost colored ring represents the community in which all three species coexist. Disturbance and
stress may positively or negatively affect energy resources (e.g., food, light), biotic interactions (e.g., competition, predation,
herbivory), and the physical (e.g., water velocity, substrate upon which an organism attaches, uses for refugia, lays eggs), or
chemical (e.g., nutrients) environment. These environmental changes may increase or decrease growth and reproduction of an
organism, consequently impacting the size and productivity of the population and interactions with other species in the community.
© 2010 Nature Education Illustrations by Summers Scholl. All rights reserved.
Isn't it Called Biomonitoring?
In common usage, the terms "biomonitoring" and "bioindication" are interchangeable, but in the scientific community these terms have
more specific meanings. Bioindicators qualitatively assesses biotic responses to environmental stress (e.g., presence of the lichen,
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Lecanora conizaeoides, indicates poor air quality) while biomonitors quantitatively determine a response (e.g., reductions in lichen
chlorophyll content or diversity indicates the presence and severity of air pollution). Hereafter, the term "bioindicator" is used as a collective
term to refer to all terms relating to the detection of biotic responses to environmental stress. Within this framework, there are three main
functions of bioindicators: 1. to monitor the environment (i.e., physical and/or chemical changes), 2. to monitor ecological processes, or 3.
to monitor biodiversity.
Examples of environmental, ecological, and biodiversity indicators can be found in many different organisms inhabiting many different
environments. Lichens (a symbiosis among fungi, algae, and/or cyanobacteria) and bryophytes (mosses and liverworts) are often used to
assess air pollution. Lichens and bryophytes serve as effective bioindicators of air quality because they have no roots, no cuticle, and
acquire all their nutrients from direct exposure to the atmosphere. Their high surface area to volume ratio further encourages the
interception and accumulation of contaminants from the air.
Figure 3: Relationship of elemental concentration within moss tissue (inset is Hylocomium splendens) to distance from the
road in Alaska, USA
Each element is represented by a different set of colored dots (red, Aluminum; yellow, Zinc; green, Lead; blue, Cadmium). The
greatest concentration of each element occurred close to the road and declined with distance from the road, demonstrating a
marked impact of overland transport of mined ore on the biota.
© 2010 Nature Education Modified from Hasselbach et al. 2005. All rights reserved.
As an example, Hasselbach et
al. (2005) used the moss Hylocomium splendens as an environmental indicator of heavy metals in
the remote tundra ecosystem of northwestern Alaska. Here, mineral ore is mined from Red Dog Mine, the world's largest producer of zinc
(Zn), and is trucked along a solitary road (~75 km in length) to storage facilities on the Chukchi Sea. Hasselbach and her colleagues
examined whether this overland transport was affecting the surrounding terrestrial biota. Heavy metal content within moss tissue was
compared at varying distances from the road (Figure 3). Metal concentrations in moss tissue were greatest adjacent to the haul road and
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decreased with distance, thus validating the hypothesis that overland transport was indeed altering the surrounding environment. In this
example, lichens were used as biomonitors, using the quantitative measurement of metal concentrations within individual lichens.
Figure 4: Aquatic macroinvertebrates document a shift in community composition related to human-induced water
withdrawals.
Bars represent the relative abundance of disturbance-intolerant taxa (green, EPT or Ephemeroptera-Plecoptera-Trichoptera), and
disturbance-adapted taxa (blue, non-insects). Line represents water discharge (Q) at each site, which significantly reduces along an
intensively managed 36-km section of the Umatilla River, Oregon, USA. Disturbance-intolerant EPT taxa markedly decline following
an 85% reduction of stream flow (far right bar). Accordingly, disturbance-adapted non-insects thrive and increase under stressed
conditions.
© 2010 Nature Education Modified from Miller et al. (2007). All rights reserved.
Similar to lichens and bryophytes, aquatic macroinvertebrates possess many of the hallmark traits of good bioindicators (Table 1). The
most common application of macroinvertebrates as bioindicators, due to their speciose nature, is at the community scale. An unimpaired
stream or river commonly contains more than 40 identifiable taxa, representing a range of habitat preferences and life history strategies.
This taxonomic and functional diversity can capture the myriad responses to different stressors and disturbances, including the presence of
fine sediment, metals, nutrients, and hydrologic alterations. Accordingly, macroinvertebrate communities have been frequently used as
environmental, ecological, and biodiversity indicators. Currently, all 50 states of the United States use aquatic macroinvertebrates to
assess the biological health of streams and rivers. For example, Miller et
al. (2007) quantified aquatic macroinvertebrates to identify a
threshold separating irrigation water withdrawals, which adversely affected the biota of river systems, from withdrawal levels that did not
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influence the community. Water withdrawals exceeding 85% of ambient levels, combined with elevated water temperatures, reduced the
proportion of disturbance-intolerant taxa, consequently shifting the community toward more disturbance-adapted species (Figure 4).
Resource managers can use the integrated response of the entire macroinvertebrate community to relate how much water can be taken for
irrigation before negative biological responses are seen, while also using the responses of individual taxa, or groups of taxa, to indicate the
mechanism(s) of environmental degradation (e.g., increased temperature or fine sediment levels) by which water withdrawals adversely
impact aquatic ecosystems. Thus macroinvertebrate populations can be used as biodiversity and ecological indicators at the community
scale and environmental indicators at the population scale.
Provide measurable response (sensitive to the
disturbance or stress but does not experience mortality or
accummulate pollutants directly from their
environment)
Good indicator ability
Response reflects the whole population/community
/ecosystem response
Respond in proportion to the degree of contamination
or degradation
Adequate local population density (rare species are
not optimal)
Abundant and common
Common, including distribution within area of question
Relatively stable despite moderate climatic and
environmental variability
Ecology and life history well understood
Well-studied
Taxonomically well documented and stable
Easy and cheap to survey
Economically/commercially
important
Species already being harvested for other purposes
Public interest in or awareness of the speces
Table 1: Regardless of the geographic region, type of disturbance, environment, or
organism, good bioindicators often share several characteristics.
Why Are Bioindicators Better Than Traditional Methods?
Scientists have traditionally conducted chemical assays and directly measured physical parameters of the environment (e.g., ambient
temperature, salinity, nutrients, pollutants, available light and gas levels), whereas the use of bioindicators uses the biota to assess the
cumulative impacts of both chemical pollutants and habitat alterations over time. Consequently, the use of bioindicators is fundamentally
different from classic measures of environmental quality and offers numerous advantages. First, bioindicators add a temporal component
corresponding to the life span or residence time of an organism in a particular system, allowing the integration of current, past, or future
environmental conditions. In contrast, many chemical and physical measurements only characterize conditions at the time of sampling,
increasing the probability of missing sporadic pulses of pollutants. In addition, contaminants can occur in exceedingly low concentrations.
Tedious analyses with highly sensitive technologies, at a prohibitive cost, are required to detect such low concentrations. Once identified,
scientists must link any potential biological hazard with these trace amounts of contaminants, when such links are largely unknown.
Alternatively, the tolerance range of bioindicators provides a picture of biologically meaningful levels of pollutants, no matter how small.
Another benefit of the use of bioindicators is their ability to indicate indirect biotic effects of pollutants when many physical or chemical
measurements cannot. Clearly, a pipe dumping phosphorus-rich sewage into a lake will adversely impact the ecosystem. Phosphorous
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commonly limits primary production in freshwater ecosystems; therefore, we may predict that elevated phosphorus concentrations will
increase the growth and reproduction of some species. Chemical measurements, however, may not accurately reflect a reduction in
species diversity or how the growth and reproduction of other species may decline due to competitive exclusion. Indirect contaminant
effects are especially difficult to glean from chemical or physical measurements in the case of bioaccumulation. Metals, among other
contaminants, accumulate in biological organisms, causing metal concentrations to amplify through food webs. Thus, contaminant levels at
higher trophic levels may be underrepresented by physical or chemical measurements.
Lastly, given the thousands of substances and factors to monitor, scientists now understand that the biota itself is the best predictor of how
ecosystems respond to disturbance or the presence of a stressor. While the use of whole communities (and all species' responses within
them) can be informative, problems can arise in especially speciose habitats. An average tropical rainforest may contain approximately 300
tree species per hectare and enumerating the response of each individual species to a disturbance is clearly unrealistic. Furthermore, a
clear bioindication signal can be obscured by an excessive number of divergent species' responses (e.g., some species may increase
while others decrease). In these cases, to integrate all the direct and indirect effects of a disturbance scientists focus only on a subset of
the biota or single species to tell the story. This narrowed approach makes monitoring more biologically relevant and cost-effective.
Moreover, a common problem with chemical and physical measurements is that they simplify a complicated response inherent in these
species-rich habitats. Bioindicators rely upon the complicated intricacies of ecosystems and use a representative or aggregated response
to convey a dynamic picture of the condition of the environment.
What Makes a Good Bioindicator?
Considering the 1.7 million species that currently documented on Earth, how do we chose just one as a bioindicator? The answer is simple:
No single species can adequately indicate every type of disturbance or stress in all environments. Depending upon the specific
environment, the species present, and local disturbances, appropriate bioindicator species or groups of species need to be selected.
Ecologists have established a broad set of criteria that species must exhibit to be considered good bioindicators (see Table 1).
Benefits and Disadvantages of Bioindicators
The numerous benefits of bioindicators have spurred legislative mandates for their use in countries around the world and their inclusion in
several international accords. Yet bioindicators are not without their problems. Like the canaries in the coal mine, we rely upon the
sensitivity of some bioindicators to function as early-warning signals. In some instances, we cannot discriminate natural variability from
changes due to human impacts, thus limiting the applicability of bioindicators in heterogeneous environments. Accordingly, populations of
indicator species may be influenced by factors other than the disturbance or stress (e.g., disease, parasitism, competition, predation),
complicating our picture of the causal mechanisms of change. A second criticism of the use of bioindicators is that their indicator ability is
scale-dependent. For example, a large vertebrate indicator (e.g., a fish) may fail to indicate the biodiversity of the local insect community.
Third, bioindicator species invariably have differing habitat requirements than other species in their ecosystem. Managing an ecosystem
according to the habitat requirements of a particular bioindicator may fail to protect rare species with different requirements. Finally, the
overall objective of bioindicators is to use a single species, or a small group of species, to assess the quality of an environment and how it
changes over time, but this can represent a gross oversimplification of a complex system.
Like all management tools, we must be conscious of its flaws. However, the limitations of bioindicators are clearly overshadowed by their
benefits. Bioindicators can be employed at a range of scales, from the cellular to the ecosystem level, to evaluate the health of a particular
ecosystem. They bring together information from the biological, physical, and chemical components of our world that manifest themselves
as changes in individual fitness, population density, community composition, and ecosystem processes. From a management perspective,
bioindicators inform our actions as to what is and is not biologically sustainable. Without the moss in the tundra, the cutthroat in the
mountain stream, and the canary in the coal mine, we may not recognize the impact of our disturbances before it is too late to do anything
to prevent them.
References and Recommended Reading
"1986:
Coal mine canaries made redundant." BBC News. December 12, 1986.
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Carignan, V. & M.-C. Villard. Selecting indicator species to monitor ecological integrity: A review. Environmental
Monitoring and
Assessment 78, 45–61 (2002).
Hasselbach, L. et
al. Spatial patterns of cadmium and lead deposition on and adjacent to National Park Service lands in the vicinity of
Red Dog Mine, Alaska. Science of the Total Environment 348, 211–230 (2005).
Iwama, G. K. et
Miller, S. W. et
al. Heat shock protein expression in fish. Reviews in Fish Biology and Fisheries 8, 35–56 (1998).
al. Resistance and resilience of macroinvertebrates to irrigation water withdrawals. Freshwater Biology 52,
2494–2510 (2007).
Rainio, J. & Niemelä, J. Ground beetles (Coleoptera: Carabidae) as bioindicators. Biodiversity
and Conservation 12, 487–506
(2003).
Rosenberg, D. M. & Resh, V. H. Freshwater
Biomonitoring and Benthic Macroinvertebrates. New York, NY: Chapman
and Hall, 1992.
Tanabe, S. & Subramanian, A. Bioindicators of POPs: Monitoring in Developing Countries. Kyoto,
Japan: Kyoto University Press, 2006.
Outline | Keywords
KEY CHALLENGES
Global Change: An Overview
Conservation of Biodiversity
EARTH'S CLIMATE SYSTEM
Introduction to the Basic Drivers of
Climate
Deep Atlantic Circulation During the Last
Glacial Maximum and Deglaciation
Geoengineering and Environmental Ethics
Milankovitch Cycles, Paleoclimatic
Change, and Hominin Evolution
BIOGEOGRAPHY: DISTRIBUTION, DISPERSAL, AND
DIVERSIFICATION OF ORGANISMS
Terrestrial Biomes
The Geography and Ecology of
Diversification in Neotropical Freshwaters
Environmental Constraints to the
Geographic Expansion of Plant and
Animal Species
Causes and Consequences of Dispersal
in Plants and Animals
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Causes and Consequences of
Biodiversity Declines
Disease Ecology
MISCELLANEOUS
Abrupt Climate Change During the Last
Ice Age
Coastal Dunes: Geomorphology
Coastal Processes and Beaches
Drip Water Hydrology and Speleothems
Earth's Earliest Climate
El Nino's Grip on Climate
Large-Scale Ecology Introduction
Methane Hydrates and Contemporary
Climate Change
Modeling Sea Level Rise
Ocean Acidification
Rivers and Streams - Water and Sediment
in Motion
Rock, Water, Microbes: Underwater
Sinkholes in Lake Huron are Habitats for
Ancient Microbial Life
Submarine Fans and Canyon-Channel
Systems: A Review of Processes,
Products, and Models
What Happens AFTER Global Warming?
SCIENTIFIC PERSPECTIVES
Principles of Landscape Ecology
Spatial Ecology and Conservation
Restoration Ecology
ECOSYSTEM PROCESSES: ENERGY FLOWS AND
BIOGEOCHEMICAL CYCLING
Energy Economics in Ecosystems
The Nitrogen Cycle: Processes, Players,
and Human Impact
Earth's Ferrous Wheel
The Ecology of Fire
Effects of Rising Atmospheric
Concentrations of Carbon Dioxide on
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Plants
METHODS IN RESEARCH AND MONITORING
Bioindicators: Using Organisms to
Measure Environmental Impacts
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