- Email: [email protected]
Biological Integrity
408 Ecological Indicators | Biological Integrity
alternative biological control approaches and for candidate agent species so that appropriate choices in methods can be made. More fundamentally, as models help refine our knowledge of the population dynamics that apply in biological control systems, our theoretical understanding of the ecology is improved. Progress in both the applied and theoretical domains offers scope to make biological control less hit-and-miss with consequent cost savings and reduced risk of environmental impact. See also: Agriculture Models; Allee Effects; Conservation Biological Control and Biopesticides in Agricultural; Growth Models; Herbivore-Predator Cycles; Insect Pest Models and Insecticide Application; Metapopulation Models; Population and Community Interactions; Predation; Prey–Predator Models; Terrestrial Arthropods.
Further Reading Barlow ND (1999) Models in biological control: A field guide. In: Hawkins BA and Cornell HV (eds.) Theoretical Approaches to Biological Control, pp. 43–68. Cambridge: Cambridge University Press. Berryman AA (1999) The theoretical foundations of biological control. In: Hawkins BA and Cornell HV (eds.) Theoretical Approaches to Biological Control, pp. 3–21. Cambridge: Cambridge University Press. Briggs CJ, Murdock WW, and Nisbet M (1999) Recent developments in theory for biological control of insects by parasitoids. In: Hawkins BA and Cornell HV (eds.) Theoretical Approaches to Biological Control, pp. 22–42. Cambridge: Cambridge University Press. Gurr GM, Barlow N, Memmott J, Wratten SD, and Greathead DJ (2000) A history of methodological, theoretical and empirical approaches to biological control. In: Gurr GM and Wratten SD (eds.) Biological Control: Measures of Success, pp. 3–37. Dordrecht, The Netherlands: Kluwer. Kean J, Wratten S, Tylianakis J, and Barlow N (2003) The population consequences of natural enemy enhancement, and implications for conservation biological control. Ecology Letters 6: 604–612.
Biological Integrity J R Karr, University of Washington, Seattle, WA, USA ª 2008 Elsevier B.V. All rights reserved.
Integrity: The Natural State Moving Biological Integrity from Concept to Measurement Selecting Metrics
Properties of a Multimetric Biological Index Application of Multimetric Biological Indexes Summary Further Reading
Integrity: The Natural State
restore and maintain the chemical, physical, and biological integrity of the nation’s waters. More recently, maintenance of biological or ecological integrity became a primary goal in diverse national and international contexts (the Canada National Parks Act, the United States’ National Wildlife Refuge System Improvement Act, the Canada–United States Great Lakes Water Quality Agreement, the European Union’s Water Framework Directive, and the Earth Charter). These initiatives have established legal, philosophical, and scientific foundations for protecting our global biological heritage. For many years, agencies and institutions responsible for implementing legislation affecting water quality neglected the biological condition of waters in favor of a focus on chemical pollutants; they assumed, erroneously, that chemical measures were an adequate surrogate of biological condition. In fact, dependence on chemical evaluations chronically underreports the extent of
Biological integrity can be defined as the presence of a balanced, integrated, adaptive biological system having the full range of parts (genes, species, and assemblages) and processes (mutation, demography, biotic interactions, nutrient and energy dynamics, and metapopulation processes) expected for locations with little recent human activity. Inherent in this definition is that (1) living systems act over a variety of scales from individuals to landscapes; (2) a fully functioning living system includes items we can count (the parts) plus the processes that generate and maintain them; and (3) living systems are embedded in dynamic evolutionary and biogeographic contexts that influence and are influenced by their physical, chemical, and biological environments. The phrase biological integrity was first used in 1972 to establish the goal of the US Clean Water Act – to
Ecological Indicators | Biological Integrity
degradation. Studies in the United States, for example, have demonstrated that chemical evaluations typically underestimate the proportion of impaired river miles by half. Because living organisms integrate the many factors operating in their environments, biological monitoring and assessment detects the complex interactions of numerous chemical pollutants, as well as degradation caused by the full array of human influences on living systems. As a result, many government agencies and citizen groups around the world are developing programs that directly monitor and assess the condition of living systems.
Moving Biological Integrity from Concept to Measurement Defining biological integrity and incorporating it into philosophical, policy, scientific, and legal constructs is but the first step toward using the concept. For credibility in any of these arenas, practitioners need tools for translating the subjective concept into something objective; they need tools both to quantify and to describe. Scientists and managers need formal methods for sampling the biota, evaluating the resulting data, and clearly describing the condition of sampled areas. A multimetric measurement system, called the index of biological integrity (IBI), developed in 1981, has helped fill this need. The complexity of biological systems and the varied impacts humans have on them require a broadly based index composed of multiple measures that, like IBI, integrates information from individual, population, assemblage, and landscape levels. If properly used, such a multimetric index enables practitioners to evaluate sites and rank them according to how far the sites diverge from integrity along a gradient of biological condition. Multimetric indexes, including conventional economic indexes such as the index of leading economic indicators, provide a convenient way to measure the status of a complex system. Such indexes typically include a variety of measurements, or metrics, that characterize the system being measured, such as housing starts or manufacturers’ shipments, inventories, and orders. Besides measuring the economy, multimetric indexes have also been developed to assess human health. Physicians apply the multimetric concept when they rely on a battery of tests to diagnose illness. Similarly, the Apgar test, developed in 1952 by anesthesiologist Virginia Apgar, assesses the condition of newborn babies on the basis of five simple criteria, including heart rate and respiration. A newborn’s scores for each criterion are summed to give an overall Apgar score ranging from 0 to 10, which describes the baby’s overall condition just after
409
birth. All multimetric indexes require a baseline state against which changing conditions are assessed. For an ecosystem, that baseline – biological integrity – is the condition at a site with a biota that is the product of evolutionary and biogeographic processes in the relative absence of the effects of modern human activity. Multimetric biological indexes integrate multiple dimensions of living systems to measure and communicate biological condition. Robust measures of the biological dimensions of site condition have by now been applied in basic science, resource management, engineering, public policy, law, and community participation on every continent except Antarctica and in developing as well as developed nations. One advantage of a robust multimetric biological index is that ecological knowledge reinforced by empirical data supports it; its use does not require resolution of all higher-order theoretical debates in contemporary ecology. Initial work to develop a multimetric approach to biological indicators concentrated on streams, with fish as focal organisms, but the underlying conceptual framework has now been applied to diverse environments (streams, large rivers, wetlands, lakes, coastal areas, coral reefs, riparian corridors, sagebrush steppe, and others) and with varied taxonomic groups (fish, aquatic and terrestrial invertebrates, algae and diatoms, birds, and vascular plants). Several US states have incorporated biological measures, or biocriteria, into state water-quality standards (Ohio, Florida, Maine, Vermont), and biological assessment is now a key component of implementing the Clean Water Act and the European Union’s Water Framework Directive.
Selecting Metrics Metrics incorporated into a multimetric biological index are chosen because they reflect specific and predictable responses of the biota to human activities across landscapes (Figure 1). These responses are similar to dose– response curves used by toxicologists, which measure how an organism’s response varies with dosage of a toxic compound. Because they provide an integrative measure of the cumulative impacts of all human activities in a region or watershed, a multimetric index and its component metrics can be viewed as ecological dose– response curves. The metrics in a multimetric index are validated empirically, and therefore they (1) are biologically and ecologically meaningful, (2) increase or decrease as human influence increases, (3) are sensitive to a range of stresses, (4) distinguish stress-induced variation from natural and sampling variation, (5) are relevant to societal concerns, and (6) are easy to measure and interpret.
410 Ecological Indicators | Biological Integrity
40
Total taxa richness
30
Clinger taxa richness
5 20
3
5 15
3
1
1 0
0
Dominance (3)
% Legless individuals 100
100
1 1
50
3 5
0 Low
High Human influence gradient
3 50 5 0 Low
High Human influence gradient
Figure 1 An example of the dose–response curves for a hypothetical four-metric IBI for a study of Japanese streams. The four metrics are benthic invertebrate taxa richness (top left); taxa richness of clinger taxa (top right); percentage of sampled individuals in sample that are legless, such as snails and worms (bottom left); and dominance, measured using the three most abundant taxa (bottom right). Black triangles represent values from reference steams considered to be minimally influenced by humans. Gray triangles represent values from highly disturbed streams. The black ovals represent a sampling site that has an IBI of 16 (3 þ 3 þ 5 þ 5). Modified from Karr JR and Chu EW (1999) Restoring Life in Running Waters: Better Biological Monitoring. Washington, DC: Island Press Copyright ª 1999 by Island Press. Reproduced by permission.
Properties of a Multimetric Biological Index Several properties of multimetric biological indexes make them particularly useful for evaluating ecosystem condition: 1. focus on biological endpoints to define condition; 2. use of reference condition (no disturbance or minimal disturbance) as a benchmark; 3. organization of sites into classes (e.g., large streams, small streams, wetlands), each with a select set of environmental characteristics; 4. assessment of change caused by human activities; 5. standardized sampling, laboratory, and analytical methods; 6. numerical scoring of sites to reflect site condition; 7. definition of condition classes, representing degrees of degradation; and 8. numerical and verbal expressions of biological condition that can be easily understood by scientists, citizens, and policy makers. Unlike single-attribute chemical measures of water quality, analytical tools such as multimetric indexes enhance practitioners’ ability to measure condition in a manner that communicates the severity and extent of biological impairment. When combined with knowledge of human activities in a study region, they also provide more effective and focused diagnostic capability to aid in defining causes of degradation. For biological assessment, most applications of purely chemical data, of tolerance indexes that measure
organisms’ tolerance of one or a few chemical pollutants, and of multivariate statistical models that yield ratios of observed to expected number of species assume, but do not demonstrate, such diagnostic power. The metrics in a multimetric index are selected to evaluate a diverse range of biological attributes, such as species richness; indicator taxa (stress intolerant and stress tolerant); relative abundances of trophic guilds and other species groups; presence of nonindigenous species; and the incidence of hybridization, disease, and anomalies such as lesions, tumors, or fin erosion (in fish) or head capsule abnormality (in stream insects). The diversity of biological signals incorporated into a multimetric index ensures that the wider consequences of human activity for living systems will be detected and understood. In addition to being scientifically rigorous, multimetric biological indexes are also policy relevant. They are, for example, sensitive enough to provide reliable assessments of both existing and emerging problems and to evaluate the effectiveness of environmental policies and programs. Integrative approaches to biological monitoring directly support efforts to attain the integrity called for in national and international policy initiatives.
Application of Multimetric Biological Indexes Multimetric biological indexes have many applications, including setting priorities for conservation, diagnosing
Ecological Indicators | Biological Integrity
the likely cause of damage at degraded sites, and evaluating the effectiveness of ecological restoration efforts. To determine a locale’s index, practitioners collect samples of invertebrates, fish, plants, or other taxa. They sort, identify, and count organisms in the sample and calculate relevant metrics, such as taxa richness or the relative abundance of species groups differentiated by pollution tolerance, taxonomic composition, functional feeding group, behavioral habit, or numerical dominance. As in the Apgar test for newborns, combining metrics into a multimetric index for bioassessment requires conversion of individual metric values into unitless numbers, or scores, which are then summed to yield a single index value. The scores are defined by comparing the locale’s metric scores with the scores expected under reference conditions, that is, at a relatively undisturbed or natural site of the same type in the same geographic region (see Figure 1). Under the IBI as originally developed, metrics can have a score of 5, 3, or 1, depending on whether the metric is comparable to, deviates somewhat from, or deviates strongly from ‘undisturbed’ reference condition. The sum of metric scores reflects the locale’s biological condition. The lowest index indicates the most-disturbed sites in poor biological condition, and the highest scores indicate relatively undisturbed sites in robust biological condition. For example, for rivers in the midwestern United States, an IBI based on 12 metrics could range from a low of 12 in areas with no fish to 60 in areas with diverse fish faunas typical of pristine locales. The benthic invertebrate IBI (B-IBI) for streams contains 10 metrics, including seven measures of taxa richness (total number of taxa; number of mayfly, stonefly, and caddisfly taxa; number of clinger, long-lived, and intolerant taxa); two relative abundance measures (predators and tolerant taxa); and dominance (relative abundance of the three most abundant taxa). B-IBI, then, ranges from 10 to 50 and defines five classes of stream conditon. In western Washington State, for example, recent work has taken two important steps in how these classes are applied: the work (1) connects the numeric
411
B-IBI, and the biological condition it reflects, to regulatory language under the Clean Water Act and (2) casts this language in terms of creatures the regional populace cares about – the Pacific Northwest’s iconic salmon (Table 1). This effort defines a stream as impaired under the act when B-IBI declines below 35, a level indicating that a stream can no longer support a healthy anadromous (migratory) salmon population. It defines a stream whose B-IBI is over 35 but under 46 as compromised but not impaired under the act. Finally, a few studies have applied the IBI approach to assessing the condition of terrestrial systems. In the shrub–steppe environments of eastern Washington and Idaho, two IBIs – one based on terrestrial invertebrates and the other on plants – were able to detect the biological effects of human actions on the resident biota. In Washington, sites with a minimal history of human disturbance had higher IBIs than all other categories of disturbance, even when that disturbance was no longer occurring (physical, waste dumping, and agricultural: Figure 2). Agricultural disturbances, whether past or present, yielded the lowest IBIs, or the poorest biological condition. A companion study in Idaho showed that biological condition was also influenced by livestock grazing and that carefully planned restoration programs increased IBIs over those at similar, unrestored sites.
Summary A key to successful restoration, mitigation, and conservation is having an objective way to measure the biological condition of sites and to compare those sites to an objectively defined benchmark condition. Multimetric biological indexes provide a tool for doing so and, at the same time, allow society to set specific biological goals for restoration programs. Moreover, because their development has incorporated ecological knowledge that has emerged in recent decades, biological indicators like IBI have fundamentally changed water resource management in many regions. Continuing work in terrestrial systems
Table 1 Benthic invertebrate index of biological integrity (B-IBI) as applied in US Pacific Northwest streams Score
Regulatory rubric
Biological condition
50–46 44–36
Healthy Compromised
34–28
Impaired
26–18 16–10
Highly impaired Critically impaired
Ecologically intact, supporting the most sensitive life forms Showing signs of degradation: impacts expected to one or more salmon life stages; loss of some intolerant, long-lived, or other taxa (e.g., stoneflies) Ecosystem parts and processes demonstrably impaired; cannot support self-sustaining salmon populations Highly inhospitable to many native fishes and invertebrates Cannot support a large proportion of native life forms; only the most tolerant taxa present
The index is partitioned into five scoring levels designed to associate regulatory language with specific biological conditions. Developed in consultation with Streamkeepers of Clallam County, Washington, USA.
412 Ecological Processes | Biological Nitrogen Fixation
Further Reading
40
Total value for IBI
30
20
10 UD
Physical Dump Disturbance category
Ag
Figure 2 The effect of disturbance type (UD, minimally disturbed; Physical, physical/chemical disturbance; Dump, sites where chemicals or debris were buried; and Ag, agricultural disturbance) on the average biological condition of shrub–steppe communities in eastern Washington, as indicated by a nine-metric IBI based on terrestrial invertebrates. Reproduced from Kimberling DN, Karr JR, and Fore LS (2001) Measuring human disturbance using terrestrial invertebrates in the shrubsteppe of eastern Washington (USA). Ecological Indicators 1: 63–81, with permission from Elsevier.
on organisms as diverse as plants, invertebrates, and birds is changing the indicator framework in terrestrial ecology as well. See also: Biomass, Gross Production, and Net Production; Connectance and Connectivity.
Davies SP and Jackson SK (2006) The biological condition gradient: A descriptive model for interpreting change in aquatic ecosystems. Ecological Applications 16: 1251–1266. European Commission (2000) Directive 2000/60/EC of the European Parliament and the Council of 23 October 2000 Establishing a Framework for Community Action in the Field of Water Policy. Official Journal of the European Communities, L327, 1–72. Brussels, Belgium: European Commission. Jungwirth M, Muhar S, and Schmutz S (eds.) (2000) Developments in Hydrobiology: Assessing the Ecological Integrity of Running Waters. Dordrecht: Kluwer Academic Publishers. Karr JR (2006) Seven foundations of biological monitoring and assessment. Biologia Ambientale 20(2): 7–18. Karr JR and Chu EW (1999) Restoring Life in Running Waters: Better Biological Monitoring. Washington, DC: Island Press. Karr JR and Kimberling DN (2003) A terrestrial arthropod index of biological integrity for shrub-steppe landscapes. Northwest Science 77: 202–213. Kimberling DN, Karr JR, and Fore LS (2001) Measuring human disturbance using terrestrial invertebrates in the shrub-steppe of Eastern Washington (USA). Ecological Indicators 1: 63–81. Natural Resources Journal (2004) Special Issue: Managing Biological Integrity, Diversity, and Environmental Health in the National Wildlife Refuges. Natural Resources Journal 44: 931–1238. Niemi GJ and McDonald ME (2004) Application of ecological indicators. Annual Reviews of Ecology, Evolution, and Systematics 35: 89–111. Pont D, Hugueny B, Beier U, et al. (2006) Assessing river biotic condition at a continental scale: A European approach using functional metrics and fish assemblages. Journal of Animal Ecology 43: 70–80. USEPA (US Environmental Protection Agency) (2005) Use of Biological Information to Better Define Designated Aquatic Life Uses in State and Tribal Water Quality Standards: Tiered Aquatic Life Uses. EPA 822-R-05-001. Office of Water. Washington, DC: US Environmental Protection Agency. Westra L (2005) Ecological integrity. In: Mitcham CD (eds.) Encyclopedia of Science, Technology, and Ethics, pp. 574–578. Detroit, MI: Macmillan.
Biological Nitrogen Fixation N Rascio and N La Rocca, University of Padua, Padua, Italy ª 2008 Elsevier B.V. All rights reserved.
Introduction Nitrogen-Fixing Organisms Nitrogenase and Nitrogen Fixation Ammonia Assimilation Symbiotic Nitrogen Fixation
Rhizobia–Legume Symbiosis Frankia-Dicotyledon Symbiosis Endophytic Diazotrophic Bacteria–Cereal Association Nitrogen Fixation in Free-Living Cyanobacteria Further Reading
Introduction
activity of photoautotrophic organisms (cyanobacteria, algae, and terrestrial plants). These primary producers take up nitrogen from the environment mainly as nitrate, reduce it to ammonia, and then assimilate ammonia into organic compounds to form amino acids. However, this process of assimilatory reduction of nitrate is not the only change that nitrogen undergoes.
Nitrogen is a key element present in many biochemical compounds (such as nucleotide phosphates, amino acids, proteins, and nucleic acids) of living cells. Only oxygen, carbon, and hydrogen are more abundant in the cell. The entry of organic nitrogen in the food chains of natural ecosystems is essentially due to the
alternative biological control approaches and for candidate agent species so that appropriate choices in methods can be made. More fundamentally, as models help refine our knowledge of the population dynamics that apply in biological control systems, our theoretical understanding of the ecology is improved. Progress in both the applied and theoretical domains offers scope to make biological control less hit-and-miss with consequent cost savings and reduced risk of environmental impact. See also: Agriculture Models; Allee Effects; Conservation Biological Control and Biopesticides in Agricultural; Growth Models; Herbivore-Predator Cycles; Insect Pest Models and Insecticide Application; Metapopulation Models; Population and Community Interactions; Predation; Prey–Predator Models; Terrestrial Arthropods.
Further Reading Barlow ND (1999) Models in biological control: A field guide. In: Hawkins BA and Cornell HV (eds.) Theoretical Approaches to Biological Control, pp. 43–68. Cambridge: Cambridge University Press. Berryman AA (1999) The theoretical foundations of biological control. In: Hawkins BA and Cornell HV (eds.) Theoretical Approaches to Biological Control, pp. 3–21. Cambridge: Cambridge University Press. Briggs CJ, Murdock WW, and Nisbet M (1999) Recent developments in theory for biological control of insects by parasitoids. In: Hawkins BA and Cornell HV (eds.) Theoretical Approaches to Biological Control, pp. 22–42. Cambridge: Cambridge University Press. Gurr GM, Barlow N, Memmott J, Wratten SD, and Greathead DJ (2000) A history of methodological, theoretical and empirical approaches to biological control. In: Gurr GM and Wratten SD (eds.) Biological Control: Measures of Success, pp. 3–37. Dordrecht, The Netherlands: Kluwer. Kean J, Wratten S, Tylianakis J, and Barlow N (2003) The population consequences of natural enemy enhancement, and implications for conservation biological control. Ecology Letters 6: 604–612.
Biological Integrity J R Karr, University of Washington, Seattle, WA, USA ª 2008 Elsevier B.V. All rights reserved.
Integrity: The Natural State Moving Biological Integrity from Concept to Measurement Selecting Metrics
Properties of a Multimetric Biological Index Application of Multimetric Biological Indexes Summary Further Reading
Integrity: The Natural State
restore and maintain the chemical, physical, and biological integrity of the nation’s waters. More recently, maintenance of biological or ecological integrity became a primary goal in diverse national and international contexts (the Canada National Parks Act, the United States’ National Wildlife Refuge System Improvement Act, the Canada–United States Great Lakes Water Quality Agreement, the European Union’s Water Framework Directive, and the Earth Charter). These initiatives have established legal, philosophical, and scientific foundations for protecting our global biological heritage. For many years, agencies and institutions responsible for implementing legislation affecting water quality neglected the biological condition of waters in favor of a focus on chemical pollutants; they assumed, erroneously, that chemical measures were an adequate surrogate of biological condition. In fact, dependence on chemical evaluations chronically underreports the extent of
Biological integrity can be defined as the presence of a balanced, integrated, adaptive biological system having the full range of parts (genes, species, and assemblages) and processes (mutation, demography, biotic interactions, nutrient and energy dynamics, and metapopulation processes) expected for locations with little recent human activity. Inherent in this definition is that (1) living systems act over a variety of scales from individuals to landscapes; (2) a fully functioning living system includes items we can count (the parts) plus the processes that generate and maintain them; and (3) living systems are embedded in dynamic evolutionary and biogeographic contexts that influence and are influenced by their physical, chemical, and biological environments. The phrase biological integrity was first used in 1972 to establish the goal of the US Clean Water Act – to
Ecological Indicators | Biological Integrity
degradation. Studies in the United States, for example, have demonstrated that chemical evaluations typically underestimate the proportion of impaired river miles by half. Because living organisms integrate the many factors operating in their environments, biological monitoring and assessment detects the complex interactions of numerous chemical pollutants, as well as degradation caused by the full array of human influences on living systems. As a result, many government agencies and citizen groups around the world are developing programs that directly monitor and assess the condition of living systems.
Moving Biological Integrity from Concept to Measurement Defining biological integrity and incorporating it into philosophical, policy, scientific, and legal constructs is but the first step toward using the concept. For credibility in any of these arenas, practitioners need tools for translating the subjective concept into something objective; they need tools both to quantify and to describe. Scientists and managers need formal methods for sampling the biota, evaluating the resulting data, and clearly describing the condition of sampled areas. A multimetric measurement system, called the index of biological integrity (IBI), developed in 1981, has helped fill this need. The complexity of biological systems and the varied impacts humans have on them require a broadly based index composed of multiple measures that, like IBI, integrates information from individual, population, assemblage, and landscape levels. If properly used, such a multimetric index enables practitioners to evaluate sites and rank them according to how far the sites diverge from integrity along a gradient of biological condition. Multimetric indexes, including conventional economic indexes such as the index of leading economic indicators, provide a convenient way to measure the status of a complex system. Such indexes typically include a variety of measurements, or metrics, that characterize the system being measured, such as housing starts or manufacturers’ shipments, inventories, and orders. Besides measuring the economy, multimetric indexes have also been developed to assess human health. Physicians apply the multimetric concept when they rely on a battery of tests to diagnose illness. Similarly, the Apgar test, developed in 1952 by anesthesiologist Virginia Apgar, assesses the condition of newborn babies on the basis of five simple criteria, including heart rate and respiration. A newborn’s scores for each criterion are summed to give an overall Apgar score ranging from 0 to 10, which describes the baby’s overall condition just after
409
birth. All multimetric indexes require a baseline state against which changing conditions are assessed. For an ecosystem, that baseline – biological integrity – is the condition at a site with a biota that is the product of evolutionary and biogeographic processes in the relative absence of the effects of modern human activity. Multimetric biological indexes integrate multiple dimensions of living systems to measure and communicate biological condition. Robust measures of the biological dimensions of site condition have by now been applied in basic science, resource management, engineering, public policy, law, and community participation on every continent except Antarctica and in developing as well as developed nations. One advantage of a robust multimetric biological index is that ecological knowledge reinforced by empirical data supports it; its use does not require resolution of all higher-order theoretical debates in contemporary ecology. Initial work to develop a multimetric approach to biological indicators concentrated on streams, with fish as focal organisms, but the underlying conceptual framework has now been applied to diverse environments (streams, large rivers, wetlands, lakes, coastal areas, coral reefs, riparian corridors, sagebrush steppe, and others) and with varied taxonomic groups (fish, aquatic and terrestrial invertebrates, algae and diatoms, birds, and vascular plants). Several US states have incorporated biological measures, or biocriteria, into state water-quality standards (Ohio, Florida, Maine, Vermont), and biological assessment is now a key component of implementing the Clean Water Act and the European Union’s Water Framework Directive.
Selecting Metrics Metrics incorporated into a multimetric biological index are chosen because they reflect specific and predictable responses of the biota to human activities across landscapes (Figure 1). These responses are similar to dose– response curves used by toxicologists, which measure how an organism’s response varies with dosage of a toxic compound. Because they provide an integrative measure of the cumulative impacts of all human activities in a region or watershed, a multimetric index and its component metrics can be viewed as ecological dose– response curves. The metrics in a multimetric index are validated empirically, and therefore they (1) are biologically and ecologically meaningful, (2) increase or decrease as human influence increases, (3) are sensitive to a range of stresses, (4) distinguish stress-induced variation from natural and sampling variation, (5) are relevant to societal concerns, and (6) are easy to measure and interpret.
410 Ecological Indicators | Biological Integrity
40
Total taxa richness
30
Clinger taxa richness
5 20
3
5 15
3
1
1 0
0
Dominance (3)
% Legless individuals 100
100
1 1
50
3 5
0 Low
High Human influence gradient
3 50 5 0 Low
High Human influence gradient
Figure 1 An example of the dose–response curves for a hypothetical four-metric IBI for a study of Japanese streams. The four metrics are benthic invertebrate taxa richness (top left); taxa richness of clinger taxa (top right); percentage of sampled individuals in sample that are legless, such as snails and worms (bottom left); and dominance, measured using the three most abundant taxa (bottom right). Black triangles represent values from reference steams considered to be minimally influenced by humans. Gray triangles represent values from highly disturbed streams. The black ovals represent a sampling site that has an IBI of 16 (3 þ 3 þ 5 þ 5). Modified from Karr JR and Chu EW (1999) Restoring Life in Running Waters: Better Biological Monitoring. Washington, DC: Island Press Copyright ª 1999 by Island Press. Reproduced by permission.
Properties of a Multimetric Biological Index Several properties of multimetric biological indexes make them particularly useful for evaluating ecosystem condition: 1. focus on biological endpoints to define condition; 2. use of reference condition (no disturbance or minimal disturbance) as a benchmark; 3. organization of sites into classes (e.g., large streams, small streams, wetlands), each with a select set of environmental characteristics; 4. assessment of change caused by human activities; 5. standardized sampling, laboratory, and analytical methods; 6. numerical scoring of sites to reflect site condition; 7. definition of condition classes, representing degrees of degradation; and 8. numerical and verbal expressions of biological condition that can be easily understood by scientists, citizens, and policy makers. Unlike single-attribute chemical measures of water quality, analytical tools such as multimetric indexes enhance practitioners’ ability to measure condition in a manner that communicates the severity and extent of biological impairment. When combined with knowledge of human activities in a study region, they also provide more effective and focused diagnostic capability to aid in defining causes of degradation. For biological assessment, most applications of purely chemical data, of tolerance indexes that measure
organisms’ tolerance of one or a few chemical pollutants, and of multivariate statistical models that yield ratios of observed to expected number of species assume, but do not demonstrate, such diagnostic power. The metrics in a multimetric index are selected to evaluate a diverse range of biological attributes, such as species richness; indicator taxa (stress intolerant and stress tolerant); relative abundances of trophic guilds and other species groups; presence of nonindigenous species; and the incidence of hybridization, disease, and anomalies such as lesions, tumors, or fin erosion (in fish) or head capsule abnormality (in stream insects). The diversity of biological signals incorporated into a multimetric index ensures that the wider consequences of human activity for living systems will be detected and understood. In addition to being scientifically rigorous, multimetric biological indexes are also policy relevant. They are, for example, sensitive enough to provide reliable assessments of both existing and emerging problems and to evaluate the effectiveness of environmental policies and programs. Integrative approaches to biological monitoring directly support efforts to attain the integrity called for in national and international policy initiatives.
Application of Multimetric Biological Indexes Multimetric biological indexes have many applications, including setting priorities for conservation, diagnosing
Ecological Indicators | Biological Integrity
the likely cause of damage at degraded sites, and evaluating the effectiveness of ecological restoration efforts. To determine a locale’s index, practitioners collect samples of invertebrates, fish, plants, or other taxa. They sort, identify, and count organisms in the sample and calculate relevant metrics, such as taxa richness or the relative abundance of species groups differentiated by pollution tolerance, taxonomic composition, functional feeding group, behavioral habit, or numerical dominance. As in the Apgar test for newborns, combining metrics into a multimetric index for bioassessment requires conversion of individual metric values into unitless numbers, or scores, which are then summed to yield a single index value. The scores are defined by comparing the locale’s metric scores with the scores expected under reference conditions, that is, at a relatively undisturbed or natural site of the same type in the same geographic region (see Figure 1). Under the IBI as originally developed, metrics can have a score of 5, 3, or 1, depending on whether the metric is comparable to, deviates somewhat from, or deviates strongly from ‘undisturbed’ reference condition. The sum of metric scores reflects the locale’s biological condition. The lowest index indicates the most-disturbed sites in poor biological condition, and the highest scores indicate relatively undisturbed sites in robust biological condition. For example, for rivers in the midwestern United States, an IBI based on 12 metrics could range from a low of 12 in areas with no fish to 60 in areas with diverse fish faunas typical of pristine locales. The benthic invertebrate IBI (B-IBI) for streams contains 10 metrics, including seven measures of taxa richness (total number of taxa; number of mayfly, stonefly, and caddisfly taxa; number of clinger, long-lived, and intolerant taxa); two relative abundance measures (predators and tolerant taxa); and dominance (relative abundance of the three most abundant taxa). B-IBI, then, ranges from 10 to 50 and defines five classes of stream conditon. In western Washington State, for example, recent work has taken two important steps in how these classes are applied: the work (1) connects the numeric
411
B-IBI, and the biological condition it reflects, to regulatory language under the Clean Water Act and (2) casts this language in terms of creatures the regional populace cares about – the Pacific Northwest’s iconic salmon (Table 1). This effort defines a stream as impaired under the act when B-IBI declines below 35, a level indicating that a stream can no longer support a healthy anadromous (migratory) salmon population. It defines a stream whose B-IBI is over 35 but under 46 as compromised but not impaired under the act. Finally, a few studies have applied the IBI approach to assessing the condition of terrestrial systems. In the shrub–steppe environments of eastern Washington and Idaho, two IBIs – one based on terrestrial invertebrates and the other on plants – were able to detect the biological effects of human actions on the resident biota. In Washington, sites with a minimal history of human disturbance had higher IBIs than all other categories of disturbance, even when that disturbance was no longer occurring (physical, waste dumping, and agricultural: Figure 2). Agricultural disturbances, whether past or present, yielded the lowest IBIs, or the poorest biological condition. A companion study in Idaho showed that biological condition was also influenced by livestock grazing and that carefully planned restoration programs increased IBIs over those at similar, unrestored sites.
Summary A key to successful restoration, mitigation, and conservation is having an objective way to measure the biological condition of sites and to compare those sites to an objectively defined benchmark condition. Multimetric biological indexes provide a tool for doing so and, at the same time, allow society to set specific biological goals for restoration programs. Moreover, because their development has incorporated ecological knowledge that has emerged in recent decades, biological indicators like IBI have fundamentally changed water resource management in many regions. Continuing work in terrestrial systems
Table 1 Benthic invertebrate index of biological integrity (B-IBI) as applied in US Pacific Northwest streams Score
Regulatory rubric
Biological condition
50–46 44–36
Healthy Compromised
34–28
Impaired
26–18 16–10
Highly impaired Critically impaired
Ecologically intact, supporting the most sensitive life forms Showing signs of degradation: impacts expected to one or more salmon life stages; loss of some intolerant, long-lived, or other taxa (e.g., stoneflies) Ecosystem parts and processes demonstrably impaired; cannot support self-sustaining salmon populations Highly inhospitable to many native fishes and invertebrates Cannot support a large proportion of native life forms; only the most tolerant taxa present
The index is partitioned into five scoring levels designed to associate regulatory language with specific biological conditions. Developed in consultation with Streamkeepers of Clallam County, Washington, USA.
412 Ecological Processes | Biological Nitrogen Fixation
Further Reading
40
Total value for IBI
30
20
10 UD
Physical Dump Disturbance category
Ag
Figure 2 The effect of disturbance type (UD, minimally disturbed; Physical, physical/chemical disturbance; Dump, sites where chemicals or debris were buried; and Ag, agricultural disturbance) on the average biological condition of shrub–steppe communities in eastern Washington, as indicated by a nine-metric IBI based on terrestrial invertebrates. Reproduced from Kimberling DN, Karr JR, and Fore LS (2001) Measuring human disturbance using terrestrial invertebrates in the shrubsteppe of eastern Washington (USA). Ecological Indicators 1: 63–81, with permission from Elsevier.
on organisms as diverse as plants, invertebrates, and birds is changing the indicator framework in terrestrial ecology as well. See also: Biomass, Gross Production, and Net Production; Connectance and Connectivity.
Davies SP and Jackson SK (2006) The biological condition gradient: A descriptive model for interpreting change in aquatic ecosystems. Ecological Applications 16: 1251–1266. European Commission (2000) Directive 2000/60/EC of the European Parliament and the Council of 23 October 2000 Establishing a Framework for Community Action in the Field of Water Policy. Official Journal of the European Communities, L327, 1–72. Brussels, Belgium: European Commission. Jungwirth M, Muhar S, and Schmutz S (eds.) (2000) Developments in Hydrobiology: Assessing the Ecological Integrity of Running Waters. Dordrecht: Kluwer Academic Publishers. Karr JR (2006) Seven foundations of biological monitoring and assessment. Biologia Ambientale 20(2): 7–18. Karr JR and Chu EW (1999) Restoring Life in Running Waters: Better Biological Monitoring. Washington, DC: Island Press. Karr JR and Kimberling DN (2003) A terrestrial arthropod index of biological integrity for shrub-steppe landscapes. Northwest Science 77: 202–213. Kimberling DN, Karr JR, and Fore LS (2001) Measuring human disturbance using terrestrial invertebrates in the shrub-steppe of Eastern Washington (USA). Ecological Indicators 1: 63–81. Natural Resources Journal (2004) Special Issue: Managing Biological Integrity, Diversity, and Environmental Health in the National Wildlife Refuges. Natural Resources Journal 44: 931–1238. Niemi GJ and McDonald ME (2004) Application of ecological indicators. Annual Reviews of Ecology, Evolution, and Systematics 35: 89–111. Pont D, Hugueny B, Beier U, et al. (2006) Assessing river biotic condition at a continental scale: A European approach using functional metrics and fish assemblages. Journal of Animal Ecology 43: 70–80. USEPA (US Environmental Protection Agency) (2005) Use of Biological Information to Better Define Designated Aquatic Life Uses in State and Tribal Water Quality Standards: Tiered Aquatic Life Uses. EPA 822-R-05-001. Office of Water. Washington, DC: US Environmental Protection Agency. Westra L (2005) Ecological integrity. In: Mitcham CD (eds.) Encyclopedia of Science, Technology, and Ethics, pp. 574–578. Detroit, MI: Macmillan.
Biological Nitrogen Fixation N Rascio and N La Rocca, University of Padua, Padua, Italy ª 2008 Elsevier B.V. All rights reserved.
Introduction Nitrogen-Fixing Organisms Nitrogenase and Nitrogen Fixation Ammonia Assimilation Symbiotic Nitrogen Fixation
Rhizobia–Legume Symbiosis Frankia-Dicotyledon Symbiosis Endophytic Diazotrophic Bacteria–Cereal Association Nitrogen Fixation in Free-Living Cyanobacteria Further Reading
Introduction
activity of photoautotrophic organisms (cyanobacteria, algae, and terrestrial plants). These primary producers take up nitrogen from the environment mainly as nitrate, reduce it to ammonia, and then assimilate ammonia into organic compounds to form amino acids. However, this process of assimilatory reduction of nitrate is not the only change that nitrogen undergoes.
Nitrogen is a key element present in many biochemical compounds (such as nucleotide phosphates, amino acids, proteins, and nucleic acids) of living cells. Only oxygen, carbon, and hydrogen are more abundant in the cell. The entry of organic nitrogen in the food chains of natural ecosystems is essentially due to the