Jump to main content.


Research Project Search
 Enter Search Term:
   
 NCER Advanced Search

2003 Progress Report: A Western Center for Estuarine Indicators Research which will Develop Indicators of Wetlands Ecosystem Health

EPA Grant Number: R828676
Center: Pacific Estuarine Ecosystem Indicator Research (PEEIR) Consortium
Center Director: Anderson, Susan L.
Title: A Western Center for Estuarine Indicators Research which will Develop Indicators of Wetlands Ecosystem Health
Investigators: Anderson, Susan L. , Allen, John , Cherr, Gary N. , Collins, Josh , Morgan, Steven , Murdoch, William W. , Nisbet, Roger M. , Pawley, Anitra , Smith, Edmund , Stewart-Oaten, Allan , Werner, I.
Current Investigators: Anderson, Susan L. , Allen, John , Bennett, Bill , Brooks, Andrew , Carr, Robert Scott , Cherr, Gary N. , Fujiwara, Masami , Green, Peter , Grosholz, Edwin , Hwang, Hyun-Min , Kendall, Bruce E. , Morgan, Steven , Murdoch, William W. , Nisbet, Roger M. , Ogle, Scott , Pawley, Anitra , Rose, Wendy , Stewart-Oaten, Allan , Swanson, Christina , Vorster, Peter
Institution: University of California - Davis , Bodega Marine Laboratory , San Francisco Estuary Institute , Smith & Associates , The Bay Institute of San Francisco , University of California - Santa Barbara
Current Institution: University of California - Davis , Pacific EcoRisk , The Bay Institute , U.S. Geological Survey , University of California - Santa Barbara , University of California - Santa Cruz
EPA Project Officer: Levinson, Barbara
Project Period: October 1, 2000 through September 30, 2004
Project Period Covered by this Report: October 1, 2002 through September 30, 2003
Project Amount: $5,998,221
RFA: Environmental Indicators in the Estuarine Environment Research Program (2000)
Research Category: Ecological Indicators/Assessment/Restoration

Description:

Objective:

The overall objective of this research project is to develop a suite of ecological indicators to assess the integrity and sustainability of wetlands in West Coast estuaries rapidly. We propose to develop an integrated suite of indicators to evaluate impacts of stressors across levels of biological organization, trophic structure, life stage, time, and space.

Progress Summary:

The Pacific Estuarine Ecosystem Indicator Research (PEEIR) Group is a consortium of 30 investigators from the University of California–Davis (UCD), the UCD Bodega Marine Laboratory (BML), and the University of California–Santa Barbara (UCSB). The overarching goal of the team is to develop indicators of wetland ecosystem health with emphasis on West Coast salt marsh systems. Our focus is on contaminant effects, but a range of stressors is considered, including: nutrient enrichment, habitat fragmentation, and pathogens. The overall design of the program includes synoptic sampling at six sites in northern and southern California. Because sampling by all investigators is conducted at precisely the same sites and stations, unprecedented integration is achieved. Other integration themes that are pursued by the entire consortium include integrative laboratory and field experiments to validate indicators and the use of model organisms for all field and laboratory investigation.

Key contributions include the development of indicators in marsh plants and animals at multiple spatial scales and levels of biological organization. These indicators are intended for various types of applications in marsh restoration, sediment quality protection, and management of specific contaminant inputs and threatened populations. There are three key integrated goals for our project. The first is the development of wetland plant indicators at multiple spatial scales and levels of organization, and the second is the development of fish and invertebrate indicators. These are described below. A third theme is an emerging effort on nutrient dynamics. The products of our program will be devised at three levels of integration with the penultimate products including synthetic recommendations on salt marsh indicators at multiple scales with succinct case studies and a comparison of synthesis techniques including multivariate statistics, modeling, and application-based suites of measurements.

Indicators in Marsh Plants

Our goal is to develop salt marsh plant indicators at multiple spatial scales and levels of biological organization, which is advantageous in providing cost-effective screening tools and diagnostic techniques to elucidate the stressors. This is an important task, because two of the key limitations of existing ecological indicators are the lack of techniques to ascribe ecological change to specific stressors and the difficulty in prioritizing problems that may occur at large spatial scales. Developing indicators at multiple scales will be advantageous because this provides both ecologically relevant and cost-effective screening tools as well as diagnostic techniques to elucidate the stressors. This is an important task, because it addresses both key limitations of existing ecological indicators: (1) the lack of techniques to ascribe ecological change to specific stressors; and (2) the difficulty in prioritizing problems that may occur at large spatial scales. Although the idea of developing indicators at multiple scales is not new, progress has been slow because development and validation of indicators must occur in a completely integrated program. Our integrated research in salt marsh plant indicators is demonstrating the utility of a Center approach to tackle a vital, but largely ignored, area (Lewis et al., 2001).

Working at the largest spatial scale, our U.S. National Aeronautics and Space Administration (NASA)-funded remote sensing team is using a variety of airborne sensors, such as the 224-band hyper-spectral AVIRIS instrument, to produce high spatial resolution data of our sites. These images and other types of remotely sensed data are being used to characterize sites with respect to patch size, disturbance, species distribution, differences in biomass, and biochemical properties including content of chlorophyll and other plant pigments, canopy water content, and dry plant litter. These data provide a previously unavailable means to characterize spatially distributed variability in species composition, physiological state, and abundance in wetlands that can be related directly to field-based chemical and physiological measurements. Understanding how these properties function as indicators is based on knowledge of physical factors, such as hydrologic and micro-topographic information, and biotic factors that we are collecting independently (e.g., using field survey techniques and LIDAR imagery). We have selected sites with varying levels of biomass, presence of contaminants, and history of disturbance within common habitats to provide a basis for comparison.

Following site selections, our plant physiologists sampled plant biomass and related indicators in the field to develop models and validate predictions. Significant effort is being devoted to comparing multiple types of metrics. We assess plant flowering, stem height, biomass, and other factors as well as photosynthetic processes using fluorometry (Juneau and Popovic, 1999) infrared gas analysis for carbon dioxide uptake, and individual spectroscopy (Bartlet et al., 1990; Gammon and Surfus, 1999; Spanglet et al., 1998; Sanderson et al., 1998; Zhang et al., 1996). Emerging technologies such as metabolomics are being applied to the plant tissues (Fan and Lane, 2000; Fan et al., 2001; Fan et al., in press, 2004a), and these will permit a phenotypic assessment of perturbations in numerous aspects of plant physiology (Colmer et al., 1996; Fan et al., in press, 2004b). The efficacy of markers varies among plant types, but because of the broad distribution of wetland species such as Salicornia and Spartina, recommendations on indicators at this level will be applicable broadly.

Because our sampling program is integrated fully, environmental chemists sampled the same plants at precisely the same locations in the sites (using DGPS) to determine whether toxicants vary in plant roots, shoots, and metal-contaminated salt exudates. These sites also are identified in the remote sensing imagery to evaluate how these stressors affect vegetation patterns in the marshes. We have sampled sites that have various levels of toxicant-related stress as well as an additional site that has a well characterized nutrient enrichment. We are using state-of-the-art analytical techniques to evaluate levels of metals and organics, but, more importantly to integrate this with ecosystem functioning. For example, the metal-contaminated salt exudation by cordgrass plants—a byproduct of osmoregulation—is an example of contaminant bioavailability that can span several spatial scales and levels of biological organization. Based on the biochemical basis of osmoregulation in these plants, we hypothesize that pollutant metal exudation by Spartina leaves will be dependent on salinity regimes and nitrogen nutrient status, potentially tying into water policies and nutrient runoff management.

In the coming year, we also will attempt to link this to variation in the structure of organic matter (OM) at our sites (Higashi et al., 1998; Fan and Lane, 2000; Fan et al., 2000), with the aim of determining whether specific OM signatures in salt marshes are predictive of toxicant bioavailability (Schultz et al., 1999), as is thought to be the case for Hg. Hence, our studies emphasize linkages between toxicant levels in sediment and bioavailability to plants (e.g., Baraud, in press). Such efforts enhance the U.S. Environmental Protection Agency’s (EPA’s) ability to develop sediment quality criteria for salt marsh systems and result in the development of specific indicators of toxic stress.

Other facets of our design include: (1) experimental studies validating physiologic responses following contaminant exposure in the laboratory; (2) additional direct linkages with other ecological responses, including nutrient cycling and microbial processing; and (3) related intensive study on mercury methylation.

We envision producing a series of highly integrated manuscripts that provide initial recommendations on indicators at each scale of organization, from biochemical to landscape. These publications will emphasize two to three case studies, but factors related to broader application will be expressed in a conceptual model. An accomplishment of this scope can only be achieved through an integrated research Center, and our team for this facet of PEEIR includes a remote sensing expert who directs a NASA Center of Excellence, two plant physiologists (among the first scientists experimenting with diverse and novel biochemical assays such as metabolomics), three innovative environmental chemists, and a geomorphologist with expertise in wetland monitoring. We believe our expertise spans an effective range from simple methodology to innovation in the most current monitoring techniques. Technology transfer is being achieved through direct linkage with EPA Region IX, the California Environmental Protection Agency, the San Francisco Bay Regional Water Quality Control Board (SFBRWQCB), the San Francisco Estuary Institute, and The Bay Institute. Our approach already has garnered significant attention, and data will be used to inform regulators (SFBRWQCB) during the restoration of Stege Marsh in San Francisco Bay and to assist in the risk assessment of mercury contamination in Tomales Bay.

Indicators in Fish and Invertebrate Model Animals

Assessment of ecological condition, diagnosis of specific stressors, and forecasting of potential changes in populations are the most significant applications of ecosystem indicators (Pretti and Cognetti-Varriale, 2001). Integrating responses of exposure to contaminants across different levels of biological organization is considered key to understanding mechanistic linkages and usefulness of indicators (Clements, 2000). These applications require the use of many types of measurements, including both stressor and ecosystem responses; yet, the options for integration of such responses are still limited (Strobel et al., 2000). A key goal of the PEEIR program is to develop a suite of integrated approaches for ubiquitous model organisms widely distributed in salt marsh ecosystems of the Pacific coast. We initially selected an invertebrate and a fish species with limited dispersal in most life stages and that inhabit mud burrows where exposure to sediment contamination is greatest, allowing us to study both within-marsh and among-marsh variations in indicators. We selected the mudsucker, Gillichthys mirabilis, as a model fish because it inhabits mud burrows and remains in the same sites (< 30 m range) for its juvenile and adult phases. The shore crab, Pachygrapsus crassipes, was chosen as the representative invertebrate, as it is highly abundant, found along the entire West coast, inhabits mud burrows, and can be found in a reproductive state during portions of the year. Limited investigations with a third species, the clam Macoma nasuta, were added in the third year to enhance the bridging between environmental chemistry and effects research, as well as to ensure that species at multiple trophic levels were represented. Investigations at the chemical, molecular, physiological, organismal, and population levels have been implemented with these three organisms, and these will result in the initial development of individual indicators as well as suites of indicators that are integrated within models and a single conceptual framework. In addition, characterization of the community structure within the habitat of these three model species also is being conducted.

Organism-level indicators are the fundamental metrics that are used to alert us to potential changes in a subpopulation at any given site. Such metrics are intuitive, and they point us to potential detrimental effects; yet, without supplemental information, they cannot inform about the potential causes of stress (Carignan and Villard, 2002). For example, if an alteration in growth or reproduction is observed, managers have little information to determine why that alteration may have occurred. Also, the absence of an observed change in growth or reproduction does not preclude changes whose primary effects are seen elsewhere in the food chain. We believe that if early warning, mechanistically-based indicators can be used to detect the stressors that managers are most concerned about, then improvements in the protection of aquatic life within a given wetland will result (Cherr, 2002; Van Dam et al., 1998; Heath, 1998).

A focus of our program is discriminating the effects of toxic substances from other habitat alterations. Hence, we directly address a limitation of previous work—the difficulty in establishing cause and effect. Prior studies typically have correlated a chemical concentration to change in a population or even simply used toxicity test data with surrogate species. Our approach is more mechanistic. Another value of our integrated indicators is that resident species, rather than surrogate test species, are used in the construction of definitive measures of chemical exposure, absorbed dose, biochemical response, and evaluation of fitness parameters including growth and reproduction. Evaluation of the growth and physiologic data in models then permits forecasting of population data into the future and can simulate varied exposure scenarios. To accomplish this goal, we have implemented an integrated program of field sampling as well as field and laboratory experiments. The program requires synoptic sampling by all investigators at all sites.

Our approach involves quantifying molecular, cellular, and biochemical responses in individual organisms collected from stressed and less-stressed wetlands, and along possible gradients within wetlands. Experiments in the field are being conducted concurrently with these efforts. This involves fish, crabs, and clams being outplanted at specific stations for up to 2 months, followed by a suite of measurements that include molecular, biochemical, and physiological parameters, which are all being linked directly to growth/condition indices at the level of individual organisms. We also are measuring contaminant levels both at the outplant sites and in tissue levels of these contaminants (bioavailability) in these organisms. Dissection teams remove appropriate tissues following field collection at well characterized sites, and they distribute these tissues to seven different investigators. Measurements include: (1) DNA strand breaks in red blood cells using the Comet assay; (2) acetylcholinesterase enzyme activity to assess organophosphate and carbamate pesticide exposure; (3) apoptosis or programmed cell death in multiple tissues; (4) metallothionein levels to evaluate metal exposure and toxicity; (5) cytochrome p450 enzymes to quantify exposure to many types of organic contaminants; (6) choriogenin proteins in male/non-reproductive fish to evaluate potential endocrine disruption; and (7) levels of metal and organic contaminants in subsets of matched fish. In addition, chemical extracts of sediment from the sites are shared among teams of analytical chemists and a molecular biology laboratory where screening for endocrine disrupting chemicals is underway. These techniques discern exposure to, and effects of, various classes of toxic substances (e.g., Huggett et al., 1992). To determine whether they are valuable indicators, variability in field sites, relation to chemical exposure, and cost and level of effort are all being considered. Multivariate analyses relating biomarker responses to growth impairment are a key part of the integration effort.

Growth rates are being compared at contaminated and reference sites and among fish with high, medium, and low biomarker responses, using daily growth increments measured in otoliths taken from the same fish used above. In addition, laboratory validation studies are underway to pinpoint selected mechanistic relationships between biomarkers and growth. We are developing new approaches based on Dynamic Energy Budget (DEB) Models (Kooijman 2000; Nisbet et al., 2000) to analyze variability in growth among individuals and assess factors that contribute to population change (Brooks, 1999). Fish growth is determined by multiple factors, so simple observation of a growth difference gives little information that managers can use with confidence. We will test whether a combination of biomarkers, growth determinations, and modeling provides a clearer picture and helps to test our understanding and confidence in the level and nature of any detrimental effect.

In parallel with the above measurements, we are conducting measurements of the ratios of stable isotopes of carbon and nitrogen at the study sites. These ratios can vary because of changes in the diet of our study animals and/or because of variations in the elemental composition of inputs to the marsh.

The DEB models of individual organisms will characterize growth and reproduction in a range of environments, and the stable isotope studies will help elucidate trophic relationships. Supplemented by information on mortality, it is possible to project (Caswell, 2001) long-term consequences on population dynamics of observed changes in individual performance. Our extensive database on population dynamics of mudsuckers over 6 years at a number of locations in the Carpinteria Marsh (Brooks, 1999) will be used as the basis of testing these projections.

As with the plant work, the animal model work has relied on a multifaceted team of chemists, molecular biologists, physiologists, fisheries scientists, and modeling experts. Two graduate students in pharmacology and toxicology, one graduate student in ecological modeling, a fisheries graduate student, and three postdoctoral researchers have been trained to work in this interdisciplinary environment. Several undergraduate assistants also have contributed to this working group. Technology transfer for this work involves extensive coordination with the SFBRWQCB, EPA Region IX, and the CALFED Bay Delta program. Our efforts will be used to inform the restoration of Stege Marsh because matching funds permit us to explicitly compare our indicators to a currently available approach that is used in management, the Sediment Quality Triad.

Modeling Work Group Summary

Individual Growth as an Indicator of Estuarine Conditions. We are evaluating potential use of differences in growth patterns in fish and invertebrates as an indicator of environmental stress. Using a stochastic DEB model, we studied possible effects of environmental variability and internal energy reserves on growth rate and size of animals (Fujiwara, et al., 2004). This theoretical study showed that more than simple summary statistics of individual growth and size data are needed to understand the effects of environmental variability on growth rate and animal size.

Motivated by the above result, we have developed a new method of fitting the stochastic individual growth model to growth data of fish and invertebrates. A complication is that the model includes internal energy reserve, which is unobservable. This difficulty was overcome by using a computer-intensive method based on non-linear forecasting to estimate model parameters.

A central assumption underpinning our use of DEB models is that the effects of sublethal levels of contaminants may be described in terms of changes in the rates of assimilation of food and of respiration by individual organisms. We are testing these assumptions—and our fitting methodology—on experiments performed by the Biological Responses to Contaminants (BRC) group on the growth of young topsmelt (Atherinops affinis) in controlled environments, where food consumption and respiration rate were measured directly. The modeling studies described above will continue. Provided technical issues relating to mudsucker otoliths are resolved, we will attempt to fit model parameters to data from natural populations and from the outplant experiments. We will start work on a population model for mudsuckers.

We will attempt some multivariate analyses on the diversity of microbial communities and the invertebrate fauna, with the aim of relating these to the stressor information obtained for some sites.

Dynamics of Stable Isotopes

PEEIR is gathering extensive data sets on carbon and nitrogen isotope ratios from many species at our study sites. Much current methodology on the interpretation of such information assumes reasonably constant conditions, not the extreme fluctuations in nitrogen supply that exist in the PEEIR study sites. We are completing a modeling study that recognizes the following facts:

Our model describes changes in nitrogen isotope ratios during growth and in the presence of external fluctuations. We disagree with one published account that says that growing and non-growing adult animals should have the same concentration of heavy nitrogen. Our results suggest that growing animals should have a lower 15N concentration than adults.

Evaluation of Index of Biological Integrity (IBI)

This work is continuing, with the issues becoming clearer with growing experience. We have reviewed the arguments by users of IBIs, with particular attention on the advantages and disadvantages of combining indicator scores into an index. Our concerns are mostly not new, though we aim to clarify them in the context of PEEIR work. The most serious is that combining measures of different things into a scalar index necessarily loses information when what you want to describe is multidimensional: if many “indicators” are indicating the same problem, we may not need all of them; if they are indicating different problems, then combining them obscures the individual information. We also are addressing some practical problems, one of which is that many IBI studies try to compare sites to an undisturbed reference, but this may not exist, and the comparison may not be appropriate. We are attempting to evaluate alternatives. We aim to develop some guidelines, more or less along decision theory lines, where remediation costs and the importance of the site (e.g., its popularity or proximity to population centers, or importance for other reasons) are considered (as they are not with IBI).

Archival Data Work Group Summary

The Ecological Scorecard. Although our theory group examines possible alternatives to the IBI, the PEEIR outreach program has partnered with Dr. Anitra Pawley at The Bay Institute to support publication of the application-based “Bay Index.” Dr. Pawley’s Bay Index takes a portfolio-type approach, establishing scores for selected management questions. Many efforts are underway to improve the health of San Francisco Bay. The Bay Institute’s Ecological Scorecard (http://www.bay.org exit EPA), released in October 2004, is intended to improve our understanding of how the entire Bay watershed is doing, to monitor how effective our stewardship of this vital resource is, and to identify future directions for management, monitoring, and research. The 2003 Bay Index focuses on the Bay itself, which is the first of four major ecological regions of the estuary—Bay, Delta, San Joaquin River and Sacramento River—proposed to be assessed as part of the Ecological Scorecard project. The Scorecard’s Bay Index uses science-based indicators to grade the condition of the Bay region: how well its ecological resources are faring, how much human activities are harming or helping the Bay, and how human uses of the Bay’s resources are affected by the Bay’s health. These indicators are combined into eight Indexes that track the Bay’s environment (Habitat, Freshwater Inflow, Water Quality), its fish and wildlife (Food Web, Shellfish, Fish), our management of its resources (Stewardship), and its direct value to the people who use it (Fishable-Swimmable-Drinkable). The grading system compares current conditions in the Bay and its watershed to historical conditions, environmental and public health standards, and restoration targets. Figure 1 provides an example of the water quality index and the composite San Francisco Bay Scorecard. PEEIR has contributed to this project, and in the upcoming year, Dr. Anitra Pawley will complete a peer-reviewed article to be submitted in the winter.

Benthic Index Review

An additional activity in PEEIR has been to review thoroughly existing benthics data for San Francisco Bay. Benthic invertebrate community measurements, particularly in the form of standardized indexes, can serve as important measures of contaminant stress and tools for effective communication of sediment quality condition to the public. Despite the fairly long history of index development in freshwater systems, the study of these areas has lagged behind those in freshwater systems so the development of indexes in estuarine system is relatively nascent. Currently, we are completing a review of the methods used to study community level benthic effects caused by contaminants, including indexes since Pearson and Rosenberg’s (1978) review of the effects of organic enrichment on marine benthic invertebrates, to address the issues that impede the development of reliable invertebrate community measures. At this time, a variety of indexes and diagnostic approaches have been proposed, each with their respective histories, strengths, and weaknesses. There are several categories of methodological techniques that are based on differences in the responses of benthic species, taxa, and functional groups to various types of anthropogenic disturbance. They include pollution scoring techniques based on species occurrences, multivariate diagnostic approaches, multimetric indexes, and the use of higher level community measures such as total species abundance, diversity, and biomass. We categorize, compare, and contrast benthic indexes and approaches, and evaluate which methods are best suited for use in variable environments. We also compare the findings derived from these studies, look for common features, and assess disagreements to provide insights to guide future research.

Ecological Scorecard

References:

Baraud F, Fan TW-M, Higashi RM. Interactive effect of cadmium and soil humates on metal acquisition and sequestration in wheat. In: Lichtfouse E, Dudd S, Robert D, eds. Environmental Chemistry (in press, 2004).

Bartlett DS, Whitting GJ, Hartman JM. Use of vegetation indices to estimate intercepted solar radiation and net carbon dioxide of a grass canopy. Remote Sensing of the Environment 1990;30:115-128.

Brooks AJ. Ph.D. Dissertation. University of California at Santa Barbara, 1999.

Carignan V, Villard MA. Selecting indicator species to monitor ecological integrity: a review. Environmental Monitoring Assessment 2002;78:45-61.

Caswell H. Matrix population models: construction, analysis and interpretation, 2nd ed. Sinauer Associates, Sunderland, MA, 2001.

Cherr GN. Can we develop and utilize indicators of ecological integrity to successfully manage ecosystems? In: Qualset CO, Rapport DJ, Ralston D, Lasley B, eds. Managing for Ecosystem Health, Third International Congress on Ecosystem Health, CRC Press, 2000, pp. 227-229.

Clements WH. Integrating effects of contaminants across levels of biological organization: an overview. Journal of Aquatic Stress and Recovery 2000;7:113-116.

Colmer TD, Fan TW-M, Läuchli A, Higashi RM. Interactive effects of salinity, nitrogen and sulphur on the organic solutes in Spartina alterniflora leaf blades. Journal of Experimental Botany 1996;47(296):369-375.

Fan TW-M, Higashi RM, Lane AN. Chemical characterization of a chelator-treated soil humate by solution-state multinuclear two-dimensional NMR with FTIR and pyrolysis-GCMS. Environmental Science and Technology 2000;34:1636-1646.

Fan TW-M, Lane AN. Nuclear magnetic resonance in analysis of plant soil environments. In: Encyclopedia of Analytical Chemistry. New York, NY: John Wiley and Sons, 2000, pp. 4082–4108.

Fan TW-M, Lane AN, Higashi RM. In vivo and in vitro metabolomic analysis of anaerobic rice coleoptiles revealed unexpected pathways. Russian Journal of Plant Physics (in press, 2004a).

Fan TW-M, Lane AN, Higashi RM. An electrophoretic profiling method for thiol-rich phytochelatins and metallothioneins. Phytochemical Analysis (in press, 2004b).

Fan TW-M, Lane AN, Shenker M, Bartley JP, Crowley D, Higashi RM. Comprehensive chemical profiling of gramineous plant root exudates using high-resolution NMR and MS. Phytochemistry 2001;57:209-221.

Gamon JA, Surfus JS. Assessing leaf pigment content and activity with a reflectometer. New Phytologist 1999;143:105-117.

Heath AG. Physiology and ecological health. In: Cech JJ, Wilson BW, Crosby DC, eds. Chelsea, MI: Lewis Publishers, 1998, pp. 59-89.

Higashi RM, Fan TW-M, Lane AN. Association of deferrioxamine with humic substances and their interaction with cadmium (II) as studied by pyrolysis-gas chromatography-mass spectrometry and nuclear magnetic resonance spectroscopy. The Analyst 1998;123:911-918.

Huggett, et al., ed. Biomarkers: biochemical, physiological, and histological markers of anthropogenic stress. A SETAC Publication, Lewis Publishers, 1992.

Juneau P, Popovic R. Evidence for the rapid phytotoxicity and environmental stress evaluation using the PAM fluorometric method: importance and future applications. Ecotoxicology 1999;8:449-455.

Kooijman S. Dynamic energy and mass budgets in biological systems, 2nd ed. Cambridge, UK: Cambridge University Press, 2000.

Lewis MA, Weber DE, Stanley RS, Moore JC. The relevance of rooted vascular plants as indicators of estuarine sediment quality. Archives of Environmental Contamination and Toxicology 2001;40:25-34.

Nisbet RM, Muller EB, Lika K, Kooijman SALM. From molecules to ecosystems through dynamic energy budget models. Journal of Animal Ecology 2000;69:913-926.

Pretti C, Cognetti-Varriale AM. The use of biomarkers in aquatic biomonitoring: example of esterases. Aquatic Conservation: Marine Freshwater Ecosystems 2001;11:299-303.

Sanderson EW, Zhang M, Ustin SL, Rejmankova E. Geostatistical scaling of canopy water content in a California salt marsh. Landscape Ecology 1998;13:79-92.

Schultz LF, Young TM, Higashi RM. Sorption-desorption behavior of phenanthrene elucidated by pyrolysis GCMS studies of soil organic matter. Environmental Toxicology and Chemistry 1999;18:1710-1719.

Spanglet H, Ustin S, Rejmankova E. Remote detection of plant community characteristics of a California subalpine marsh. Wetlands 1998;18 (3):307-319.

Strobel CJ, Paul JF, Hughes MM, Buffum HW, Brown BS, Summers JK. Using information on spatial variability of small estuaries in designing large-scale estuarine monitoring programs. Environmental Monitoring Assessment 2000;63:223-236.

Van Dam RA, Camilleri C, Finlayson CM. The potential of rapid assessment techniques as early warning indicators of wetland degradation: a review. Environmental Toxicology Water Quality 1998;13:297-312.

Zhang M, Ustin SL, Rejmankova E, Sanderson EW. Remote sensing of salt marshes: potential for monitoring. Ecological Applications 1996;7(3):1039-1053.

Future Activities:

See the future activities included in the individual 2004 Annual Reports for the subprojects of R828676, R828676C001- R828676C003.


Journal Articles: 34 Displayed | Download in RIS Format

Other center views: All 133 publications 35 publications in selected types All 34 journal articles

Type Citation Sub Project Document Sources
Journal Article Anderson SL, Cherr GN, Morgan SG, Vines CA, Higashi RM, Bennett WA, Rose WL, Brooks A, Nisbet RM. Integrating contaminant responses in indicator saltmarsh species [short communication]. Marine Environmental Research 2006;62(Suppl. 1):S317-S321. R828676 (Final)
R828676C002 (Final)
not available
Journal Article Córdova-Kreylos AL, Cao Y, Green PG, Hwang HM, Kuivila K, LaMontagne MG, Van De Werfhorst LD, Holden PA, Scow KM. Diversity, composition, and geographical distribution of microbial communities in California salt marsh sediments. Applied and Environmental Microbiology 2006;72(5):3357-3366. R828676 (Final)
R828676C003 (Final)
not available
Journal Article Fan TWM, Lane AN, Higashi RM. An electrophoretic profiling method for thiol-rich phytochelatins and metallothioneins. Phytochemical Analysis 2004;15(3):175-183. R828676C003 (2003)
R825960 (Final)
not available
Journal Article Fan TWM, Lane AN, Chekmenev E, Wittebort RJ, Higashi RM. Synthesis and physico-chemical properties of peptides in soil humic substances. Journal of Peptide Research 2004;63(3):253-264. R828676C003 (2003)
not available
Journal Article Field KG, Chern EC, Dick LK, Fuhrman J, Griffith J, Holden PA, LaMontagne MG, Le J, Olson B, Simonich MT. A comparative study of culture-independent, library-independent genotypic methods of fecal source tracking. Journal of Water and Health 2004;1(4):181-194. R828676 (Final)
R828676C003 (Final)
R827639 (Final)
not available
Journal Article Fleming EJ, Mack EE, Green PG, Nelson DC. Mercury methylation from unexpected sources: molybdate-inhibited freshwater sediments and an iron-reducing bacterium. Applied and Environmental Microbiology 2006;72(1):457-464. R828676C003 (2004)
R829388C001 (2005)
  • Abstract from PubMed
  • Full-text: AEM Full Text
    Exit EPA Disclaimer
  • Other: AEM PDF
    Exit EPA Disclaimer
  • Journal Article Fujiwara M, Kendall BE, Nisbet RM. Growth autocorrelation and animal size variation. Ecology Letters 2004;7(2):106-113. R828676 (2003)
    R828676 (2004)
    R828676 (Final)
    not available
    Journal Article Fujiwara M, Kendall BE, Nisbet RM, Bennett WA. Analysis of size trajectory data using an energetic-based growth model. Ecology 2005;86(6):1441-1451. R828676 (Final)
    R828676C001 (2004)
    not available
    Journal Article Green PG, Fan TW-M, Higashi RM. Salt exudations from coastal wetland plants as a measure of metal mobilization from sediment. Environmental Toxicology and Chemistry (submitted, 2004). R828676C003 (2003)
    not available
    Journal Article Gurney WSC, Nisbet RM. Resource allocation, hyperphagia and compensatory growth. Bulletin of Mathematical Biology 2004;66(6):1731-1753. R828676 (2004)
    R828676 (Final)
    not available
    Journal Article Hechinger RF, Lafferty KD. Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society B: Biological Sciences 2005;272(1567):1059-1066. R828676 (Final)
    R828676C001 (2004)
    R828676C003 (Final)
    not available
    Journal Article Huspeni TC, Lafferty KD. Using larval trematodes that parasitize snails to evaluate a saltmarsh restoration project. Ecological Applications 2004;14(3):795-804. R828676 (Final)
    R828676C001 (2002)
    R828676C003 (Final)
    not available
    Journal Article Hwang H-M, Green PG, Higashi RM, Young TM. Tidal salt marsh sediment in California, USA. Part 2: Occurrence and anthropogenic input of trace metals. Chemosphere 2006;64(11):1899-1909. R828676 (Final)
    not available
    Journal Article Lafferty KD, Holt RD. How should environmental stress affect the population dynamics of disease? Ecology Letters 2003;6(7):654-664. R828676C001 (2002)
    not available
    Journal Article Lafferty KD, Hechinger RF, Lorda J, Soler L. Trematodes associated with mangrove habitat in Puerto Rican salt marshes. Journal of Parasitology 2005;91(3):697-699. R828676C001 (2004)
    not available
    Journal Article Lafferty KD, Dunham EJ. Trematodes in snails near raccoon latrines suggest a final host role for this mammal in California Salt Marshes. Journal of Parasitology 2005;91(2):474-476. R828676C001 (2004)
    not available
    Journal Article Lafferty KD. Is disease increasing or decreasing, and does it impact or maintain biodiversity? Journal of Parasitology. R828676C001 (2002)
    not available
    Journal Article Lafferty KD, Porter JW, Ford SE. Are diseases increasing in the ocean?. Annual Review of Ecology Evolution and Systematics 2004;35():31-54 R828676C001 (Final)
    not available
    Journal Article LaMontagne MG, Holden PA. Comparison of free-living and particle-associated bacterial communities in a coastal lagoon. Microbial Ecology 2003;46(2):228-237. R828676 (Final)
    R828676C003 (2003)
    R828676C003 (Final)
    not available
    Journal Article LaMontagne MG, Leifer I, Bergmann S, Van De Werfhorst L, Holden PA. Bacterial diversity in marine hydrocarbon seep sediments. Environmental Microbiology 2004;6(8):799-808. R828676 (Final)
    R828676C003 (2003)
    R828676C003 (Final)
    not available
    Journal Article Li L, Ustin SL, Lay M. Application of multiple endmember spectral mixture analysis (MESMA) to AVIRIS imagery for coastal salt marsh mapping: a case study in China Camp, CA, USA. International Journal of Remote Sensing 2005;26(23):5193-5207. R828676 (Final)
    R828676C003 (Final)
    not available
    Journal Article Magalhaes C, Bano N, Wiebe WJ, Hollibaugh JT, et al. Comparison of ammonium oxidizing bacterial phylotypes and function between biofilms and sediments of the Douro River Estuary, Portugal. Environmental Microbiology (in review, 2005). R828676C001 (2004)
    not available
    Journal Article Morgan SG, Spilseth SA, Page HM, Brooks AJ, Grosholz ED. Spatial and temporal movement of the lined shore crab Pachygrapsus crassipes in salt marshes and its utility as an indicator of habitat condition. Marine Ecology Progress Series 2006;314:271-281. R828676 (Final)
    R828676C001 (Final)
    not available
    Journal Article Pillai MC, Vines CA, Wikramanayake AH, Cherr GN. Polycyclic aromatic hydrocarbons disrupt axial development in sea urchin embryos through a β-catenin dependent pathway. Toxicology 2003;186(1-2):93-108. R828676C002 (2003)
    not available
    Journal Article Rose WL, Hobbs JA, Nesbit RM, Green PG, Cherr GN, Anderson SL. Validation of otolith growth rate analysis using cadmium-exposed larval topsmelt (Atherinops affinis). Environmental Toxicology & Chemistry 2005;24(10):2612-2620. R828676 (Final)
    R828676C002 (2004)
    not available
    Journal Article Rosso PH, Ustin SL, Hastings A. Mapping marshland vegetation of San Francisco Bay, California, using hyperspectral data. International Journal of Remote Sensing 2005;26(23): 5169-5191. R828676 (Final)
    R828676C003 (Final)
    not available
    Journal Article Rosso PH, Pushnick JC, Lay M, Ustin SL. Reflectance properties and physiological responses of Salicornia virginica to heavy metal and petroleum contamination. Environmental Pollution 2005;137(2):241-252. R828676 (Final)
    not available
    Journal Article Rosso PH, Ustin SL, Hastings A. Use of lidar to study changes associated with Spartina invasion in San Francisco Bay marshes. Remote Sensing of Environment 2006;100(3):295-306. R828676 (Final)
    R828676C003 (Final)
    not available
    Journal Article Shaw J, Aguirre-Macedo L, Lafferty KD. An efficient strategy to estimate intensity and prevalence: sampling metacercariae in fishes. Journal of Parasitology 2005;91(3):515-521. R828676C001 (2004)
    not available
    Journal Article Spilseth SA, Morgan SG. Evaluation of internal elastomer tags for small, mature crabs. Crustaceana 2005;78(11):1383-1388. R828676 (Final)
    R828676C001 (2004)
    R828676C001 (Final)
    R825689C028 (Final)
    not available
    Journal Article Steets BM, Holden PA. A mechanistic model of runoff-associated fecal coliform fate and transport through a coastal lagoon. Water Research 2003;37(3):589-608. R828676 (Final)
    R828676C003 (2002)
    R828676C003 (Final)
    not available
    Journal Article Ward JR, Lafferty KD. The elusive baseline of marine disease: are diseases in ocean ecosystems increasing? PLoS Biology 2004;2(4):542-547. R828676C001 (2003)
    not available
    Journal Article Gurney WSC, Jones W, Veitch AR, Nisbet RM. Resource allocation, hyperphagia, and compensatory growth in juveniles. Ecology 2003;84(10):2777-2787. R828676 (Final)
    not available
    Journal Article Hwang H-M, Green PG, Young TM. Tidal salt marsh sediment in California, USA. Part 1: Occurrence and sources of organic contaminants. Chemosphere 2006;64(8):1383-1392. R828676 (Final)
    not available
    Supplemental Keywords:

    watersheds, estuary, ecological effects, bioavailability, ecosystem indicators, aquatic, integrated assessment, EPA Region IX, , Ecosystem Protection/Environmental Exposure & Risk, Geographic Area, Scientific Discipline, Waste, RFA, Ecosystem/Assessment/Indicators, exploratory research environmental biology, Aquatic Ecosystems & Estuarine Research, Bioavailability, Ecological Risk Assessment, Aquatic Ecosystem, Ecological Indicators, Ecological Effects - Environmental Exposure & Risk, Ecosystem Protection, Ecology and Ecosystems, State, biomarkers, ecosystem condition, water quality, California (CA), ecosystem indicators, ecosystem health, environmental indicators, environmental stressor, environmental consequences, wetlands, fish , statistical evaluation, GIS, plant indicator, ecological exposure, aquatic ecosystems, biological indicators, biological markers, ecosystem integrity, environmental stress, Western Center for Estuarine Research, ecological assessment, estuaries, estuarine ecosystems, biomarker
    Relevant Websites:

    http://www.bml.ucdavis.edu/peeir/program.html exit EPA

    Progress and Final Reports:
    2001 Progress Report
    Original Abstract
    2004 Progress Report
    Final Report

    Subprojects under this Center: (EPA does not fund or establish subprojects; EPA awards and manages the overall grant for this center).
    R828676C000 Pacific Estuarine Ecosystem Indicator Research (PEEIR) Consortium: Administration and Integration Component
    R828676C001 Pacific Estuarine Ecosystem Indicator Research (PEEIR) Consortium: Ecosystem Indicators Component
    R828676C002 Pacific Estuarine Ecosystem Indicator Research (PEEIR) Consortium: Biological Responses to Contaminants Component: Biomarkers of Exposure, Effect, and Reproductive Impairment
    R828676C003 Pacific Estuarine Ecosystem Indicator Research (PEEIR) Consortium: Biogeochemistry and Bioavailability Component

    Top of page

    The perspectives, information and conclusions conveyed in research project abstracts, progress reports, final reports, journal abstracts and journal publications convey the viewpoints of the principal investigator and may not represent the views and policies of ORD and EPA. Conclusions drawn by the principal investigators have not been reviewed by the Agency.


    Local Navigation


    Jump to main content.