Response of a benthic food web to hydrocarbon contamination

Direct and indirect effects of diesel-contaminated sediment on microalgae, meiofauna, and meiofauna-microalgae trophic interactions were examined in a microcosm study of the sediment community from a Spartina aZterniJora salt marsh. Microcosms of natural sediment were given small daily doses of contaminated sediment over a 28-d period, creating low-, medium-, and high-diesel treatment concentrations of -0.5, 5.5, and 55 ppm PAH, respectively. Diesel caused initial (within 7 h) reductions in microalgal grazing by meiobenthic harpacticoid copepods. Over longer periods of exposure (7-28 d), grazing on microalgae by copepods as a group was reduced in highdiesel treatments, primarily because of high copepod mortality. In contrast, grazing by and abundance of Cletocamptus deitersi (a copepod) was significantly enhanced in high-diesel treatments. Concurrent with reduced grazing by copepods, nematode grazing rates increased significantly in high-diesel treatments, indicating possible competition for microalgae between copepods and nematodes. In spite of transiently enhanced grazing by nematodes and C. deitersi, total meiofaunal grazing on microalgae was reduced in high-diesel treatments. Increased Chl a: pheopigment ratios in contaminated sediments were also indicative of reduced grazing pressure. A large (10X) increase in microalgal biomass was observed in high-diesel treatments and was likely a consequence of reduced meiofaunal grazing. The general responses observed in microcosms were also observed in a field study of polycyclic aromatic hydrocarbon contamination. Collectively, our data indicate that benthic microalgal biomass is controlled by meiofaunal grazing and that meiofauna may compete for limited algal resources. Furthermore, consideration of multiple trophic levels and their interactions allows a more complete and ecologically meaningful understanding of the mechanisms by which contaminants induce changes in natural communities. In shallow coastal systems microphytobenthos are considered to be an important food source for benthos and provide the principal source of nutrition that fuels secondary production in general (Sullivan and Moncreiff 1990). Trophic relationships between sedimentary microalgae and their potential consumers are, however, complex and poorly understood (Miller et al. 1996). Microalgal biomass may be reduced by macrofaunal grazing pressure (e.g. Connor et al. 1982; Darley et al. 1981; Pace et al. 1979), indicating that microalgal biomass is limited by grazing pressure. Nutrients (usually N; Darley et al. 1981; Posey et al. 1995) or light (Estrada et al. 1974) may also limit microalgal growth. Some studies indicate positive feedback between macrofaunal grazers and microalgae at moderate grazer densities (Bianchi and Rice 1988; Connor et al. 1982). Nilsson et al. (1991) determined that nutrient availability was the primary factor controlling microalgae, and that meiofaunal grazing had a minimal impact on microphytobenthos. We are unaware of other previous manipulative experimental work concerning the control of microalgae by meiofaunal grazing, but based on comparisons of meiofaunal grazing rates and microalgal productivity, it has been suggested that meiofauna, particularly copepods, may control benthic microalgal biomass and Acknowledgments Several undergraduate and graduate students assisted with this project, including B. Hughes, T Huynh, G. Lotufu, M. McCall, M. Pace, S. Rai, and B. Sun. A. Todaro assisted with copepod identifications. E. Chesney and l? Sammarco graciously provided access to facilities at the LUMCON facility. The manuscript was improved by comments from L. Levin and two anonymous reviewers. The research was supported by grants from the Office of Naval Research (N00014-93-l-0975), Minerals Management Service (14-35-000130660), and the Department of Energy. that meiofauna may be limited by availability of microalgal food (Blanchard 1991; Montagna et al. 1995b). Meiofauna may in turn be regulated by predation by juvenile fish, shellfish, and infauna (Gee 1989). An understanding of benthic food-web relationships has implications not only for fundamental ecology but also for properly interpreting and predicting the effects of environmentalor contaminant-induced perturbations because effects at one trophic level (fish, invertebrates, or microalgae) could lead to responses at another level. Such indirect effects (e.g. “trophic cascades,” top-down or bottom-up effects) are common in planktonic aquatic communities in general (Wootton 1994) and may also occur in the benthos (Kneib 199 1; Posey et al. 1995). Contaminants may influence a food web in a manner similar to that of a predator. For example, if a contaminant reduces grazer consumption of primary production (either through grazer mortality or sublethal effects), an ecological manifestation of the contaminant will be an increase in primary-producer biomass (if the primary producer is not limited by other factors). Thus, a complete understanding of the effects of the contaminant requires analysis not only of responses by grazers and primary producers per se but also of trophic interactions between the two. Here, we examine the effect of diesel-contaminated sediments on the meiofaunal-microalgal food web of a coastal salt marsh. Diesel fuel is considered to be highly toxic because it is enriched in polycyclic aromatic hydrocarbons (PAH; National Toxicology Program 1986), the most toxic component of petroleum hydrocarbons (Clark 1989; Kennish 1992). Studies of environmental impacts of oil spills, controlled petroleum amendments in microcosms and field settings, and laboratory bioassays indicate that PAH can reduce diversity, density, or reproductive success of meiofauna, but