Grantee Research Project Results
2002 Progress Report: Integrative Indicators of Ecosystem Condition and Stress across Multiple Trophic Levels in the San Francisco Estuary
EPA Grant Number: R827644Title: Integrative Indicators of Ecosystem Condition and Stress across Multiple Trophic Levels in the San Francisco Estuary
Investigators: Dugdale, Richard C. , Kimmerer, Wim , Arp, Alissa J. , Thompson, Janet K. , Bollens, Stephen Morgan , Wilkerson, Frances P. , Julian, David William
Institution: San Francisco State University
Current Institution: San Francisco State University , U.S. Geological Survey - Sacramento , University of Florida
EPA Project Officer: Packard, Benjamin H
Project Period: October 1, 1999 through September 30, 2002 (Extended to September 30, 2003)
Project Period Covered by this Report: October 1, 2001 through September 30, 2002
Project Amount: $881,062
RFA: Ecological Indicators (1999) RFA Text | Recipients Lists
Research Category: Aquatic Ecosystems , Ecological Indicators/Assessment/Restoration
Objective:
The overall objectives of this research project are to: (1) establish the utility of the potential indicators of ecosystem condition at three stations along a salinity gradient in the San Francisco Estuary; (2) investigate relationships of indicators to variations, in other physical (e.g., temperature, salinity, turbidity) and biological (e.g., introduced species, copepod prey for herring) parameters; and (3) assess the utility of the ecological indicators for use in other locations. The specific objectives of this research project are to establish: (1) nutrient status and productivity performance of phytoplankton including the relative contribution of diatoms to phytoplankton biomass and productivity; (2) reproductive rates of common copepod (zooplankton) species; (3) nutritional condition of larval Pacific herring using morphometric characters, some of which are sensitive to growth (food), e.g., body weight, and some of which are relatively insensitive to growth (food), e.g., eye diameter; (4) changes in benthic community structure and growth rate, condition, and glycogen content of key benthic organisms; and (5) the use of molecular tools to evaluate conditions in benthic bivalves, larval herring, and copepods.
This research is being conducted on the open-water ecosystem of the San Francisco Estuary, including the portion of the landscape from freshwater to marine ecosystems (i.e., Suisun, San Pablo, and Central Bays). These potential indicators represent key population and individual-level processes in a variety of trophic levels, and cover planktonic and benthic communities. All indicators relatively are simple to measure, significant to population ecology, expected to be sensitive to stress levels, and likely are transportable to other aquatic habitats.
Progress Summary:
Nutrient/Phytoplankton Indicator Study
Throughout the study, we have measured temperature, salinity, nutrients, and chlorophyll every month during cruises that occupied three stations in the San Francisco Bay along a salinity gradient (Suisun Bay: USGS Station 6, San Pablo Bay: USGS Station 13, and Central Bay: RTC Station XB-D). In addition, these stations also were sampled weekly during times when phytoplankton "blooms" occur (i.e., March, April, and October). In our proposed research, we planned to assess the "health" or condition and production of the phytoplankton community by evaluating the nutrient status and relative contribution to the phytoplankton community by diatoms, and by comparing phytoplankton productivity carried out under in situ light conditions with optimal conditions of increased light. However, this study actually revealed relevant information about the nature of the nitrogen compounds used in the estuary, or regulated phytoplankton growth and success. Consequently, we focused more in Year 3 on the regulatory impact of ammonium (NH4) concentrations on phytoplankton production. We continued to conduct incubations to compare in situ versus optimal growth rates (using 15N) as proposed, but these data will be analyzed in detail later this year, as our mass spectrometer has now been repaired.
As in prior years, elevated chlorophyll biomass levels (i.e., blooms-indicating a "healthy condition") were dominated by larger cells, typically diatoms. The nutrient status in the estuary indicates nonlimiting conditions for nitrate (NO3) and silicate for phytoplankton growth. However, the relative concentrations of NO3 and NH4 may be important in determining if the non-limiting NO3 concentrations actually are available to the phytoplankton. Ammonium concentrations measured in the San Francisco Bay during this study often were high and in the range (> 4 µM) known to inhibit the uptake of NO3 by phytoplankton (especially diatoms). Our tracer (15N) measurements of NO3 and NH4 uptake by phytoplankton in Suisun, San Pablo, and Central NH4 levels fall below inhibitory levels. The spring diatom bloom, a major primary production event in the Bay, is the result of this burst of NO3 uptake. However, the pattern of spring blooms in the three bays is variable both in timing and intensity; all three may show spring blooms, only the lower bays may bloom, or all three bays may show no blooms in a given year. This variability in primary production may be the result of the interaction between the major sources of NH4 to the bay, from treatment plant effluent, agricultural drains, and the amount of spring runoff or freshwater flow. In dry years, up to 80 percent of the inorganic nitrogen supply to the bay is from the two anthropogenic sources. In the future, we expect that dry years, or situations with reduced flow resulting from water management, will result in low NO3 uptake and diatom production, and that wet (especially El Niño) conditions will be associated with high NO3 uptake and phytoplankton blooms. It is likely that 2003 will be an El Niño year and may offer wet conditions to test this.
Zooplankton Indicator Study
During Year 3, we completed our research cruises and have finished analysis of samples from all but three of the cruises. We also have completed two experiments in which the reproductive rate was measured with excess food as cultured phytoplankton. So far, reproductive rates under these conditions have not been as high as those observed during some of the cruises. This suggests that other food (e.g., ciliates) may be important in the diet of Acartia spp., which is in agreement with other studies from various locations, including the San Francisco Estuary.
We have not found any evidence that salinity affects reproductive rate in the field. Evidently, when salinity is too low for reproduction, the populations are so sparse as to preclude measuring reproductive rate, which requires a fairly abundant population.
We also have found an apparent discrepancy in reproductive rates among copepods, depending on whether they were carrying spermatophores (these are sperm sacs that indicate recent mating; however, according to the literature, Acartia, females can store sperm from a single mating and need not mate more than once). This unexpected result complicates inferences about environmental controls on reproduction. We will attempt to account for it by reexamining copepods for spermatophores and calculating rates separately for those that had clearly mated and those whose mating status is unknown. This will reduce the effective number of copepods included in the calculations, but may reduce the (considerable) variability among individuals, particularly when reproductive rates are fairly high.
Condition Indices of Larval Pacific Herring (Clupea pallasi)
Once a month, between November and May, we collected triplicate net tows at two stations (San Pablo Bay and Central Bay). We sorted, identified, and measured the anal body depth (mm), pectoral body depth (mm), eye diameter (mm), standard length (mm), head width (mm), and dry weight (mg) of 902 herring larvae, and derived nine indices of condition for each larva. We were able to determine that three of the nine derived indices of condition (i.e., Body Weight/Eye Diameter, Body Weight/ Standard Length, and Body Weight/Head Width) appear to be driving the variation in the data set. Therefore, these three show the greatest promise as indicators of larval herring condition. Through multivariate analysis, we have identified spatial (location) and temporal (seasonal and interannual) separation between the indices, suggesting that they may be useful in identifying trends in larval herring condition. There does not appear to be a strong correlation between larval herring condition and either chlorophyll biomass or copepod egg production rates. However, we are exploring this further.
Benthic Indicators Study
Monthly collections of benthic community, glycogen, and condition samples continued to be collected at one central bay site, two San Pablo Bay sites, four Suisun Bay sites, and one Grizzly Bay site. Although there continues to be some argument about the presence of exotic species in a system indicative of ecosystem stress, there is little argument that once a new species is established, it can induce stress. It is less certain which invasive species likely will result in ecosystem level changes. We have documented the benthic community and ecosystem changes that have occurred with the invasion of one exotic bivalve, Potamocorbula amurensis. With the completion of our analysis of one heavily invaded station, P. amurensis was one of seven exotic species to invade this community during the study period 1977-2000. We have established some questions that can be used to judge if a benthic species is likely to change and stress an ecosystem. These questions include the following: Is the exotic species likely to persist in time (i.e., is the species at a physiological limit within the new environment)? Is the exotic species geographically widespread? Can it reproduce throughout its geographic range? Does the species dominate the biomass of its feeding functional group and the benthic community? If so, is the change in biomass sufficient to change the impact of this functional feeding group on the ecosystem? Can the species directly change the success of other organisms by limiting or enhancing the success of organisms with specific reproductive strategies or specific environmental requirements (e.g., living on the surface or only in the subsurface)? Can the combination of all of these factors result in a change in the transfer of contaminants within the food web? In our analyses of the benthic community at this long-term monitoring station, we found that, unlike the other six exotic species that also invaded this community, P. amurensis possesses all of these attributes. P. amurensis: (1) has a broad environmental tolerance and the San Francisco Bay is in the middle of its latitudinal range; (2) spreads and is capable of reproducing throughout the system; (3) has increased the biomass of its functional feeding group (filter feeder) by one to two orders of magnitude and now dominants the biomass of the benthic community; (4) is capable of consuming larvae of species with pelagic larvae, thereby decreasing their abundance; (5) enhances populations of organisms without pelagic larvae, which are capable of feeding from multiple food sources by increasing the food supply within and on the surface of the sediment; and (6) increases the availability of some contaminants to higher trophic levels because of their physiological ability to store some contaminants, their high biomass, and their surface dwelling habits which make them very accessible. A comparison of these traits with other successful benthic invaders (Corbicula fluminea and Dreissena polymorpha) that have resulted in ecosystem level changes, has been encouraging.
Use of Condition and Glycogen as Stress Indicators
Our analyses of glycogen content in bivalves shows that there is a relationship to food availability, and that P. amurensis responds quickly to an increase in food by building up its energy reserves. The combination of condition and glycogen continues to show promise as an indicator of environmental stress on this community.
Physiological Indicators Study
We now have fully characterized the levels of four key stress proteins in P. amurensis tissues obtained from benthic study sites 4.1, 6.1, 8.1, and 12.5, from February 6, 2001 to July 17, 2001. These stress proteins are heat shock protein 60 (hsp60), mitochondrial small heat shock protein (shsp), and mitochondrial manganese superoxide dismutase (MnSOD). The homogenized samples are in storage in an ultra-cold freezer.
Our analyses up to this point indicate that there are significant differences in expression of these stress proteins, at different sites and times during the study period. In general, animals from site 4.1 had the lowest levels of stress proteins at all times, while animals at site 8.1 generally had the highest levels (except MnSOD, which was low in animals from that site). Overall, stress protein levels were typically lowest during April and May. Some sites showed particularly strong interactions. For example, animals at site 8.1 showed a strong increase in both hsp60 and hsp70 at site during March 2001, and an increase in mitochondrial shsp at site 8.1 from May to July 2001.
Future Activities:
The no-cost extension was requested to enable data analysis to continue and, in particular, to investigate relationships of indicators/data collected concerning condition to variation in other physical (e.g., temperature, salinity, and turbidity) and biological (e.g., introduced species, copepod prey for herring) parameters. Future activities include:
Phytoplankton. Mass spectrometry of Years 2 and 3 will continue, so that analyses of the light enhanced productivity experiments can be evaluated for use as a "stress" indicator. We will continue monthly sampling and tracer experiments at the three sites in the San Francisco Bay for physical variables (salinity, temperature, and turbidity), nutrients, phytoplankton biomass, and composition and productivity, until ship-time costs are expended (probably until May 2003). In addition, small enclosure experiments to track NO3 versus NH4 uptake kinetics and to investigate NO3/NH4 interactions and their impact on phytoplankton productivity and composition will be conducted.
Zooplankton. In spring 2003, we plan to conduct sampling to capture the phytoplankton bloom. During that time, we will refine our estimates of food limitation and make estimates of availability of alternative food that could support high reproductive rates. Additionally, samples will be analyzed and results will be documented.
Larval Herring. Future activities include sampling for larval herring in the San Pablo Bay and Central Bay locations from November 2001 through May 2002. Future research will involve further investigation of the relationship between larval condition indices and physical and other biological indices, to develop ecosystem-level indices of condition.
Benthic Studies. We have begun applying the same techniques used with the Grizzly Bay benthic data to the San Pablo Bay benthic data to assess the changes and effects of changes on the ecosystem in the benthic community. In combining our knowledge of stress on this community, as reflected in our glycogen and condition data, we predict a smaller amount of stress levels. This will test our questions about assessing the stress of exotic species on ecosystems because there are several exotic species in this community. We are in the process of writing a journal publication of Heather Peterson's thesis that summarizes her findings in Grizzly Bay.
Stress Proteins. The sample analysis we have completed so far is still too short to draw firm conclusions about trends. However, we have recently obtained samples from Dr. Thompson from those same four sites (see results above) for the subsequent 18-month collection period, and we are processing those tissues for subsequent analyses. We anticipate completing these analyses by the end of summer 2003. At that time, we will look for correlations between individual stress protein expression levels and the other indicators of ecosystem and population stress obtained by the other studies within this project.
Journal Articles on this Report : 1 Displayed | Download in RIS Format
Other project views: | All 53 publications | 3 publications in selected types | All 1 journal articles |
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Type | Citation | ||
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Parchaso F, Thompson JK. Influence of hydrologic processes on reproduction of the introduced bivalve Potamocorbula amurensis in northern San Francisco Bay, California. Pacific Science 2002;56(3):329-345. |
R827644 (2002) R827644 (Final) |
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Supplemental Keywords:
marine, estuary, ecological effects, organism, ecosystem, indicators, aquatic, western, pacific coast, California, CA, phytoplankton, zooplankton, benthos, morphometrics., RFA, Scientific Discipline, Water, Geographic Area, Ecosystem Protection/Environmental Exposure & Risk, Nutrients, Ecology, Ecosystem/Assessment/Indicators, Ecosystem Protection, Environmental Chemistry, State, Chemistry, Ecological Effects - Environmental Exposure & Risk, Microbiology, EPA Region, aquatic ecosystem, environmental monitoring, nutrient supply, EMAP, marine ecosystem, Region 9, stressors, trophic transfer, bioavailability, phytoplankton dynamics, ecosystem indicators, salinity, bioindicators, aquatic ecosystems, benthos-associated organisms, San Franciso Estuary, ecological indicators, California (CA), benthic nutrients, populationRelevant Websites:
http://userwww.sfsu.edu/~bioocean/research/epaherring/epaherring.html Exit
http://userwww.sfsu.edu/~phytopl/ Exit
http://www.zoo.ufl.edu/julian/ Exit
http://online.sfsu.edu/~kimmerer/research.htm Exit
Progress and Final Reports:
Original AbstractThe 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.