Grantee Research Project Results
Final 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 , 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 Amount: $881,062
RFA: Ecological Indicators (1999) RFA Text | Recipients Lists
Research Category: Aquatic Ecosystems , Ecological Indicators/Assessment/Restoration
Objective:
The objectives of this research project were to:
- Establish the utility of developing indicators of ecosystem condition at three stations along a salinity gradient in the San Francisco Estuary. These include:
- Nutrient status (importance of NH4 versus NO3 to the dissolved inorganic nitrogen pool) and productivity performance of phytoplankton, including the relative contribution of diatoms to phytoplankton biomass and productivity.
- Reproductive rates of common copepod (zooplankton) species.
- 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).
- Changes in benthic community structure and growth rate, condition, and glycogen content of key benthic organisms.
- Using molecular tools to evaluate condition in benthic bivalves, larval herring, and copepods.
- Investigate relationships of indicators to variation in other physical (e.g., temperature, salinity, turbidity) and biological (e.g., introduced species, copepod prey for herring) parameters.
- Assess the utility of the ecological indicators for use in other locations.
This research was conducted in 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). The indicators represent key population- and individual-level processes in a variety of trophic levels and cover planktonic and benthic communities. All indicators are relatively simple to measure, significant to population ecology, are sensitive to stress conditions, and are transportable to other aquatic habitats.
Summary/Accomplishments (Outputs/Outcomes):
Nutrient/Phytoplankton Indicator Study
Throughout the study, monthly measurements of temperature, salinity, nutrients, and chlorophyll were made during cruises that occupied three stations in San Francisco Bay along a salinity gradient (Suisun Bay: U.S. Geological Survey (USGS) Station 6; San Pablo Bay: USGS Station 13; and Central Bay: RTC Station XB-D. These stations also were sampled weekly during times when phytoplankton “blooms” were likely to occur (i.e., March-April and October). In our proposed research we planned to assess the “health” or condition of the phytoplankton community and production 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, in collecting the data to test these proposals, this study actually revealed relevant information about the nature of the nitrogen compounds in the estuary that are used or regulate phytoplankton growth and success. Consequently, we focused more in the last year on the regulatory impact of ammonium (NH4) concentrations on phytoplankton production.
In all years of the study, elevated chlorophyll biomass levels (i.e., blooms—indicating a “heathy condition”) were dominated by the larger cells, typically diatoms. The nutrient status in the estuary indicated nonlimiting conditions for nitrate (NO3) and silicate for phytoplankton growth (i.e., levels generally above 20 µM). However the availability of the NO3 was restricted when high levels of NH4 occurred; that is, relative concentrations of NO3 and NH4 may be important in determining whether the nonlimiting NO3 concentrations actually are available to the phytoplankton. NH4 concentrations measured in San Francisco Bay during this study were often 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 showed that NO3 uptake was almost always low or undetectable in all three bays except during the spring diatom bloom ( a major primary production event in the Bay) that results from a 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, from agricultural drainage 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. The long decline in fisheries and productivity in San Francisco Bay may be a result of the change in sewage treatment practice, from primary to secondary treatment and the increased NH4 concentrations in effluents.
Consequently, the research carried out suggests that NH4 concentration is a primary indicator of impaired phytoplankton productivity in San Francisco and probably in many other estuaries as well. A threshold value of 3 mM NH4 was apparent in our data for “healthy” chlorophyll production. Below that value, high values of chlorophyll occurred and NO3 uptake was greater than that of NH4. The NH4 concentration was also a predictor of the f-ratio (i.e. the nitrate use, described as the proportion of NO3 uptake to NO3 plus NH4 uptake). Low NH4 concentrations were correlated with high f-ratios and high chlorophyll concentrations. High f values are characteristic of eutrophic high new production conditions and high yields of fisheries in the coastal ocean. f-ratios typically are low in San Francisco Bay when NH4 concentrations are high, as occurs most of the time and most places, even though there is ample NO3. A low NH4 concentration does not guarantee bloom formation that also requires sufficient irradiance to drive photosynthesis.
Research in which bay water is enclosed and exposed to natural irradiance has shown that normal, fast uptake of NO3 and production of chlorophyll will commence as soon as NH4 concentrations fall to low levels. All NO3 then will be taken up within 3-4 days, as observed also in “healthy” coastal upwelling ecosystems. This length of time also may be used as an indicator. If NO3 uptake following NH4 exhaustion exceeds the 3-4 day indicator limit, there may be some negative factor (e.g., heavy metal toxicity, poor irradiance conditions, etc.) that is preventing “health” nutrient depletion rates by the phytoplankton. These concepts and data have been presented at many national meetings and included in a submitted manuscript, a newsletter report, and an almost complete manuscript comparing the interannual variability of the 3-year data set.
Zooplankton Indicator Study
We completed 36 experiments examining the joint effect of food and salinity on egg production rate by copepods of the genus Acartia and estimated egg production rates of Limnoithona tetraspina, Oithona davisae, and O. similes using samples from 20 cruises. We also have completed two experiments in which reproductive rate was measured with excess food as cultured phytoplankton. 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., in agreement with other studies from various locations, including the San Francisco Estuary. At this point we consider the maximum field-based estimates to represent the maximum possible for the three Acartia species collected.
On reanalyzing our entire data set we found once again that Acartia egg production was strongly responsive to food but found that there was a slight depressive effect of lowered salinity on egg production rate. However, because it was rather subtle, we do not believe that egg production provides an adequate indicator of salinity stress, at least under the conditions of these experiments. Nevertheless, this was one of the most comprehensive field-based analysis of copepod egg production ever completed.
Egg production of Limoithona and Oithona spp. was low and unresponsive to food or salinity. This is consistent with data from elsewhere on Oithona spp., although there are no studies on Limnoithona for comparison. These data form the basis for a manuscript about to be submitted to Marine Ecology Progress Series.
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 and so 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 a biomass or copepod egg production rates. The spatial separation between the indices was confirmed through analysis of covariance, which points to potentially important differences between Central and San Pablo Bays as nursery grounds for larval herring (Bollens and Sanders, 2004). These data were published in American Fisheries Society Symposium.
Benthic Indicators Study
Monthly collections of benthic community, glycogen, and condition samples were completed 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 being indicative of ecosystem stress, there is little argument that once a new species is established that it can induce stress. It is less certain which invasive species are likely to 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: (1) Is the exotic species likely to persist in time (i.e., is the species at a physiological limit within the new environment)? (2) Is the exotic species geographically widespread? Can it reproduce throughout its geographic range? (3) Does the species dominate the biomass of its feeding functional group and of the benthic community? If so, is the change in biomass sufficient to change the impact of this functional feeding group on the ecosystem? (4) 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)? (5) 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 that the San Francisco Bay is in the middle of its latitudinal range, (2) spread throughout the system and is capable of reproducing throughout the system, (3) has increased the biomass of its functional feeding group (filter feeder) by 1-2 orders of magnitude and now dominants the biomass of the benthic community, (4a) is capable of consuming larvae of species with pelagic larvae thereby decreasing their abundance, (4b) enhanced populations of organisms without pelagic larvae that are capable of feeding from multiple food source by increasing the food supply within and on the surface of the sediment, and (5) has increased 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 that 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. Condition patterns proved to be very volatile and not easily related to stress. 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. Glycogen concentrations in bivalves increased with increasing salinity, between the freshwater end station and Carquinez Straits, then remained steady or slightly declining in animals through San Pablo Bay. It is possible that this pattern could reflect freshwater stress in animals at the freshest station, but previous years’ data at that station showed the highest glycogen concentrations during the one of the wettest years on record. This pattern is most likely consistent with animals being food limited in the channels. A limited amount of phytoplankton may be supplied by the shallow portions of Suisun Bay as in the past and thus areas adjacent to the shallow reaches of Grizzly Bay may benefit from this food supply. It is more likely that phytoplankton are tidally transported upstream from San Pablo Bay, which may have a higher phytoplankton biomass than Suisun Bay, thereby augmenting the food supplies to bivalves at the most downstream channel stations (e.g., Carquinez St.). The higher glycogen levels at the Sand Bar (adjacent to the channel) supports both of these hypotheses. The shallower water at this location may make it easier for the bivalves to filter more particles because of the higher vertical mixing rate in shallower water. Glycogen concentration has some promise as an indicator of relative health of bivalves in a estuary. They must, however, be taken over several seasons and at several locations with the same species at all locations for the index to be useful. Condition does not appear to have any utility as an index of estuarine stress in this system.
Stress Protein Study
After 2 years of effort, we were ultimately unsuccessful in obtaining reproducible two-dimensional gel electrophoresis analyses of tissue samples from P. amurensis. As a result, we reverted to one-dimensional gels and Western blots to analyze key stress proteins. This was the plan originally outlined in the grant proposal, although we have elected to analyze four proteins instead of just two. The stress proteins we selected are manganese super-oxide dismutase (MnSOD), heat shock protein 60 (HSP60), heat shock protein 70 (HSP70), and small heat shock proteins (sHSP). Heat shock proteins (HSPs) are protein chaperones that are present in virtually all animals thus far examined. These proteins generally function to suppress protein aggregation. In both vertebrates and invertebrates, HSP expression increases following exposure to a variety of stressors, including heat, heavy metal contamination, hypoxia, oxidative stress, and in some cases hyposalinity. HSP60 is primarily mitochondrial, whereas HSP 70 and the sHSPs are both mitochondrial and cytosolic.
We now have prepared homogenates and analyzed protein contents of tissues from 41 collections at sites 4.1, 6.1, 8.1, and 12.5 from February 7, 2001, to May 8, 2002. The homogenized samples are in storage in an ultra-cold freezer. We have analyzed expression of HSP60, HSP 70, sHSP, and MnSOD for animals from all sites from February 7, 2001, through July 17, 2001. The remaining samples have been assayed for expression of these proteins, but the data have not yet been quantified and analyzed.
From February 7, 2001, through July 17, 2001, clams from site 8.1 typically had increased HSP60, HSP70, and sHSP expression at all time points compared to the other sites. For HSP60 and HS70, this pattern was most evident in the February 2001 collection, at which time the animals had 1.5x higher expression than at the other sites. For sHSPs, the higher expression was especially marked from May 2001 and later, when sHSP expression in animals from site 8.1 was more than 2-fold higher than that of animals from any other site. All animals showed very low expression of all HSPs in the April 2001 collection. Also note that sHSP expression in animals from all sites other than 8.1 was similar and relatively invariant.
MnSOD catalyzes the conversion of the extremely damaging superoxide radical to the less toxic hydrogen peroxide, which is then converted to water and oxygen by catalase. MnSOD expression is increased following exposure to stressors suspected to induce oxidative stress, including hypoxia-reoxygenation and heavy metals. Expression of MnSOD in P. amurensis showed no clear pattern from February 7, 2001, through July 17, 2001, although animals from site 6.1 typically had the highest expression levels.
In most cases where there was a strong difference in expression of stress proteins among sites for a specific date, site 4.1 showed the lowest expression levels. This could indicate either that clams at this site were under the least stress or that clams at this site were under so much stress that they were unable to mount an adequate stress protein response following stress exposure. Overall, our stress protein data suggest the former, with site 4.1 being the least stressful and site 12.5 being the most stressful overall during February 7, 2001 through July 17, 2001. These results will need to be cross-referenced with data on glycogen content and condition to determine whether these stress proteins provide correlates of these more traditional indicators of organism health.
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, biology, aquatic, ecology, monitoring, 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.