Identifying Benthic Indicators for San Francisco Bay Sarah Lowe and Bruce Thompson San Francisco Estuary Institute, Oakland, CA Introduction   Background Literature Review Results Discussion References

Introduction

Since its inception in 1994, the objective of the RMP Benthic Pilot Study has been to evaluate the use of benthic information for determining environmental conditions in the Estuary. Previous Annual Report articles have summarized the species composition and distribution of benthic assemblages and their relationship with salinity and sediment-types. They have also discussed the issue of defining ambient reference benthic conditions in the Estuary. In this article we describe the process used to identify benthic indicators which can be used to identify both impacted and ambient reference benthic assemblages (unimpacted benthic communities) in the San Francisco Estuary. We also discuss the potential and the problems of using these benthic indicators and other biological variables to evaluate test sites for contaminant effects.

Background

Biomonitoring is commonly used to assess changes in the environment. A common method of evaluation is to compare biological variables from test sites to those from reference sites. Typically, a test sample is considered to be impacted if one or more biological indicators are "significantly" different from those of the reference conditions. The key to such a strategy is the clear understanding of reference conditions.

Benthic assemblages in the San Francisco Estuary respond to many types of physical, chemical, and biological fluctuations. The Estuary experiences natural fluctuations due to variations in freshwater flows, salinity, and sedimentation, as well as historic and recurring anthropogenic influences including nutrient and organic enrichment, and contamination. It is difficult to identify a benthic response to contamination when contamination commonly covaries with many of these other environmental factors (Nichols, 1979; Peterson et al., 1996; Swartz et al., 1986; Spies et al., 1988). Additionally, most of the benthic species that currently inhabit the Estuary are non-native species (Cohen and Carlton, 1995), therefore, large amounts of information about the changes in benthos in space and time, and the corresponding changes in environmental and contaminant factors are required to observe consistent patterns and trends (Luoma and Carter, 1991).

Identifying truly unimpacted reference locations within the Estuary is probably not possible and no other nearby estuary has characteristics similar to the San Francisco Estuary which could serve as a true "reference" location for biological comparisons. Therefore, "ambient" reference locations must be identified from the existing benthic monitoring data. An "ambient" reference benthic assemblage is defined as:

A sample of organisms that currently inhabit the least-contaminated areas of the Estuary that includes species known (from studies elsewhere) to inhabit uncontaminated sediments, but do not include very many species known to inhabit contaminated sediments. These assemblages should exhibit natural fluctuations in species composition and abundance in response to changes in salinity and sediment-type.

Literature Review

There have been several published studies of benthic species responses to contamination in San Francisco Bay including: Filice, 1959; Nichols, 1979; Chapman et al., 1987; Lee et al., 1994; Hunt et al., 1998. Additionally, studies of benthic responses to contamination in other locations have been used to identify the types and abundances of benthic organisms one might expect to find in unimpacted and impacted areas in the Estuary. The use of literature as an initial step avoids the common assumption that if sediments are contaminated then the benthos must be impacted. No a priori assumptions about sediment contamination in the Estuary are required in applying the findings from the literature.

The goal of the literature search was to create a list of benthic species (or higher taxa) that inhabit the San Francisco Estuary and have been shown to be indicators of either unimpacted or impacted conditions. The literature search included studies from around the world. We queried the University of California, Berkeley BIOSIS library database for relevant information about the 460 species identified in the 1994­1996 Benthic Pilot Studies.

Benthic impacts from contamination have typically been broadly defined to include both organic enrichment (nutrients) and contaminants which often occur together in runoff and effluent. Many articles reported organismal response to sediments containing contamination and organic enrichment, or other disturbances. Articles that reported responses exclusively to organic enrichment or other disturbances were not included. Most articles concurred in their characterization of a taxon, but a few articles were contradictory and professional judgment was used in categorizing or including the following taxa: Corbicula fluminea, Corophium acherusicum, Euphilomedes sp., Mediomastus sp., Podarke obscura, and Streblospio benedicti (see Table 4.1).

Results

Indicators of Salinity and Sediment-type

Based on Benthic Pilot Study data collected between 1994 and 1996, several benthic assemblages have been identified (Thompson et al., 1997). Species composition and abundance in those assemblages generally reflect differences in salinity and sediment-types in the Estuary. The most common and abundant species in each assemblage are listed on Table 4.1. Those species may be considered to be indicators of environmental conditions from which they were collected. For example, the amphipod Corophium spincorne only occurs in the Fresh Brackish assemblage where salinities are below about 5 psu, in fine sediments, whereas another closely related amphipod Corophium insidiosum occurs only in the Central Bay assemblage, where salinities are above 30 psu, in fine sediments. Similarly, the worm Heteropodarke sp. was only collected at Red Rock in very sandy sediments, thus is an indicator of high salinity and sandy sediments.

Indicators of Ambient Reference and Impacted Conditions

The results of the classification and ordination analyses presented in last year's RMP Annual Report provide preliminary information about impacted and unimpacted assemblages in the Estuary. We identified a contaminated sub-assemblage of the Estuarine assemblage that had reduced numbers of species and individuals, as well as indicators of contamination (e.g., Streblospio benedicti). In that case, the analysis was able to distinguish a difference in species composition and abundance in the China Camp (RMP Wetlands Pilot Study) and Castro Cove (Bay Protection and Toxic Cleanup Program; BPTCP) samples from RMP samples from the adjacent Estuarine assemblage (see the 1996 RMP Annual Report for further explanation). In the Central Bay, the two Bay Area Dischargers Associations, Local Effects Monitoring Program (BADA LEMP) sites, City and County of San Francisco (CCSF), and East Bay Municipal Utility District (EBMUD), were classified as part of the Central Bay assemblage. However, the analyses could not distinguish any difference between those samples and Central Bay samples farther from the discharge.

In both examples, no sediment contamination information was included. However, it has not been conclusively demonstrated that any of the major assemblages are more characteristic of unimpacted or impacted conditions. As shown by RMP sediment contamination monitoring, all sites have moderate amounts of contamination (see sediment sections). The above examples demonstrate the need for unbiased assessment based on indicators alone.

The results of the literature search characterized 30% of all taxa identified in the 1994­1996 Benthic Pilot Study. These taxa are listed in Table 4.2 and comprise half of the ten most common and abundant species found in each benthic assemblage in the Estuary (Table 4.1). Capitella "capitata" is one of the most well known marine pollution indicators and has been found to be tolerant of a wide variety of contaminants including trace metals, hydrocarbons, and general pollution (Levin et al., 1996; Bridges et al., 1994; Plante-Cuny et al., 1993; Daan et al., 1996; Peterson et al., 1996; Daan et al., 1994; Chapman et al., 1987; Pearson and Rosenberg, 1978; BPTCP, 1996; Tetra Tech, 1990; Milbrink, 1980; Raman, 1995; Holte et al., 1996). Another polychaete, Streblospio benedicti, has been found to tolerate hydrocarbon contamination (Levin et al., 1996; Chandler et al., 1997; Chapman et al., 1987; Pearson and Rosenberg, 1978; Dauer, 1993; BPTCP, 1996; Bridges et al., 1994). Polychaetes in the family Dorvilleidae and Eteone sp. are present in polluted waters and can often be found along with Capitella and Streblospio (Pearson and Rosenberg, 1978; Thompson, 1982; Milbrink, 1980; Tetra Tech, 1990). The oligochaete Limnodrilus hoffmeisteri was shown to be tolerant of various types of contaminants including high sediment concentrations of pyrene and phenanthrene (Lotufo and Fleeger, 1996; Simpson et al., 1993; Lang and Reymond, 1996; Matagi, 1996; Lafont et al., 1996; Martinez and Levinton, 1996; Montuelle et al., 1997; Peterson et al., 1996; Dauer, 1993; Pearson and Rosenberg, 1978). References for nematodes included variable conclusions; one article showed that they were tolerant to PAHs, while another showed they were intolerant to cadmium, and a third showed that different species had variable tolerances to contamination (Carman et al., 1995; Chandler et al., 1994; Hansen et al., 1996; Peterson et al., 1996).

Contaminant intolerant species include most amphipod crustaceans and some harpactacoid copepods which are highly sensitive to toxic chemicals (Peterson et al., 1996; DeWitt et al., 1988; Word et al., 1977; Swartz et al., 1994). Ampelisca abdita, a dominant amphipod in the San Francisco Estuary, is quite sensitive to contamination (Ferraro and Cole, 1997; Swartz et al., 1994). Other amphipod species, such as Corophium acherusicum, are also good indicators of uncontaminated environments (Tetra Tech, 1990; Pearson and Rosenberg, 1978; Flemer et al., 1997; Ferraro and Cole, 1997; Swartz et al., 1994). Unlike most other amphipods, Grandidierella japonica is tolerant of contamination (Ferraro and Cole, 1997; Swartz et al., 1994; Carr et al., 1996). Since amphipods are dominant members of all major assemblages in the Estuary (Table 4.1), they are very good candidates for ambient reference indicators.

Echinoderms, especially brittlestars, occur in the Central Bay and are also very sensitive to contamination (Thompson, 1982; Peterson et al., 1996; Milbrink, 1980; Word et al., 1977; Swartz et al., 1986). Based on examination of RMP data collected to date, echinoderms do not inhabit sites where the salinity is below 15 psu. Therefore, echinoderms would only be useful ambient reference indicators for the Central Bay assemblages.

The introduced Asian clam Potamocorbula amurensis is often dominant in the Estuary. Studies by the U.S. Geological Survey have shown that it is sensitive to metals contamination (Parchaso et al., 1997; Thompson et al., 1996; Brown and Luoma, 1995). Several articles about Corbicula fluminea suggested it is useful for bioaccumulation studies, but they were inconclusive in characterizing it as a potential benthic indicator (Hayward et al., 1996; Moulton et al., 1996; Foe and Knight, 1986). However, it appears that the larvae are adversely affected by contaminants (Boltovskoy et al., 1997).

Abundances of some higher taxa have been used as indicators. Proportions of oligochaetes (small worms) and chironomids (aquatic insects) have been used to characterize freshwater communities where they generally increase in abundance with increased contamination (Canfield et al., 1994; 1996). Oligochaetes of the family Tubificidae are generally classified as contaminant tolerant indicators, but some genera are contaminant intolerant; for example Spirosperma and Varichaetadrilus pacificus (Canfield et al., 1994). The genus Pristina (oligochaete family Naididae) was also cited as being intolerant to industrial pollution (Lafont et al., 1996). Oligochaetes are found throughout the Estuary although their abundance increases at freshwater sites. Chironomids are restricted to freshwater (<2 psu) and thus, would only be good indicators in the Fresh Brackish assemblage. The relative proportions of copepods to nematodes has also been used. The proportion increases with increased contamination (Peterson et al., 1996).

It is not obvious how to apply the information about each indicator species. Generally, no guidelines exist as to the exact abundance of an indicator that would distinguish impacted from unimpacted sites. The percentage of all impacted or unimpacted indicator taxa or abundances identified could be used. However, since information was not found for all species collected in the Estuary, those estimates would be imprecise.

Other commonly used biological indicators are the number of taxa, total abundances, and total biomass of a sample (Pearson and Rosenberg, 1978; Swartz et al., 1986). However, the use of those variables has several problems in their application. First, there are no guidelines as to which exact values one should expect from an ambient reference site (although once reference sites are identified using other indicators, ranges could be calculated as described in the discussion section). More importantly, those indicators are not usually linearly related to contamination (including organic enrichment). Instead, biological indicators, such as the number of taxa, total abundance, and biomass, often are higher in locations where there is moderate contamination. This phenomenon is known as "intermediate disturbance" and has also been observed in tropical rain forests and coral reefs where other types of disturbance have a similar effect (Connell, 1986). Intermediate disturbance is an initial response to environmental disturbances such as the influx of effluent which might contain both nutrients and contaminants. Under such conditions, it is believed that nutrient benefits dominate over contaminant effects (provided that the contamination is not too high) and benthic populations increase and diversify (Figure 4.19). At some threshold along the contamination gradient, contaminant effects become too great and the community begins to decline. Where non-linear responses occur, a biological indicator could have the same value at an unimpacted and an impacted site (Figure 4.19), an undesirable quality for an indicator. At severely impacted sites, very low numbers of species and abundance would be expected.

Discussion

The Benthic Pilot Study data and the literature review have provided information about many of the species that inhabit San Francisco Bay and whether they might serve as indicators of unimpacted ambient reference conditions or indicators of contamination impacts. The types and number of taxa, total abundances, and the number of indicator taxa should reveal information about the condition of sediments without making any a priori assumptions based on the sediment contamination found at a site.

Based on our literature review and current understanding of changes in the benthic community response to contamination in the San Francisco Estuary, several benthic variables are being evaluated as candidate indicators of ambient reference conditions:

• amphipod abundances (except G. japonica),
• echinoderm abundances (where salinity is above 15 psu),
• abundances of unimpacted indicator taxa.

Several other variables are being evaluated as candidate indicators of impacted conditions:

• elevated abundances of oligochaetes,
• elevated abundances of chironomids (where salinity is below 2 psu),
• abundances of impacted indicator taxa.
  

The selection of appropriate benthic indicators for the Estuary should consider whether candidate indicators actually respond to changes in contamination, but the RMP has apparently not sampled any severely contaminated sites. These phenomena need to be understood before indicators can be used. Analyses conducted to date have shown that understanding some of the indicators responses is complicated. Some examples of unresolved issues are listed below.

• What proportion of taxa indicative of impacted conditions would make a sample "significantly" different from ambient reference conditions?
• At Redwood Creek, echinoderms are collected in some samples but not others, although the salinity and sediment-type is similar. Does that reflect contaminant effects or life history phenomenon?
• What triggered the large influx of the amphipod Corophium ascherusicum in August 1995 in the Central Bay and their subsequent demise?
  

Most investigators have used numerical approaches to create a "benthic index" that is calibrated to distinguish impacted from unimpacted samples (O'Connor and Swanson, 1982; Word et al., 1977; Tetra Tech, 1990; Weisberg et al., 1992; Smith et al., 1988). A benthic index was used in the BPTCP for San Francisco Bay samples based on the presence or absence of several benthic indicator species (Hunt et al., 1998).

Another approach, based on the range of reference values, has been used for both sediment chemistry and toxicity in the Estuary (see articles by Hunt et al. and Gandesbery et al. in this report). Typically, a test sample may be considered significantly different from a reference condition if the value of an indicator (e.g., number of amphipods) is outside of a chosen percentile reference confidence limit. Any percentile could be chosen and is a subjective decision. But, there must be some justification for choosing a specific percentile. Alternatively, the simple range of amphipod abundance at ambient reference sites could be used, but there is no statistical confidence associated with a simple range.

The use of tolerance limits for a set of benthic indicators is being evaluated. However, preliminary calculations have shown that in most cases, the number of samples used as ambient reference samples for each assemblage is too low to yield useful tolerance limits. Additionally, more information about contaminated samples is needed. Additional information will facilitate the identification of suitable benthic indicators.

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