An integrated assessment of polycyclic aromatic hydrocarbons (PAHs) and benthic macroinvertebrate communities in Isle Royale National Park

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Abstract

Polycyclic aromatic hydrocarbons (PAHs) are a class of persistent organic pollutants that are known carcinogens and mutagens. This research used the sediment quality triad, an integrated weight-of-evidence approach, to evaluate sediment PAH concentrations, sediment toxicity, and benthic community structure at marina and reference sites in Isle Royale National Park, USA. The highest PAH concentrations were measured at marina locations and exceeded threshold effect concentrations (161 μg PAH/g TOC) at one site. Marina locations were dominated by pyrogenic PAHs, indicating anthropogenic sources of these compounds. Survival of the amphipod Hyalella azteca was significantly reduced (p = 0.0320) when exposed to sediments from marinas. Although macroinvertebrate abundance and species richness were similar at marina and reference sites, results of multivariate analyses showed that composition of benthic communities varied among sites. In particular, abundance of the PAH-sensitive amphipod, Diporeia spp. was significantly lower at marina sites compared to reference sites. In contrast to patterns observed for organochlorines (e.g., PCBS, dioxins), biota-sediment accumulation factors for PAHs measured in the burrowing mayfly Hexagenia limbata decreased with increasing Kow values, suggesting that the more lipophilic compounds were being metabolized. Increased PAH concentrations, shifts in community composition, low survival of H. azteca, and reduced abundances of Diporeia spp. at marina sites were consistent with the hypothesis that PAHs impacted these areas; however, across all sites these effects were relatively subtle. These results emphasize the need to use a weight-of-evidence approach when investigating effects of environmental contaminants that occur at relatively low concentrations.

Highlights

► Concentrations of PAHs in sediment from marinas exceeded the threshold effect level. ► Survival of Hyalella azteca was reduced when exposed to sediments from marinas. ► Macroinvertebrate abundance and richness were similar at reference and marina sites. ► Abundance of PAH-sensitive amphipods (Diporeia spp.) was reduced at marinas. ► A weight-of-evidence approach was required to demonstrate ecological effects.

Introduction

Polycyclic aromatic hydrocarbons (PAHs) are a class of persistent organic pollutants consisting of 2 to 6 fused aromatic rings that are produced from both natural and anthropogenic sources. Pyrogenic PAHs (4 to 6 rings) are a result of incomplete combustion of organic material at high temperatures (> 500 °C) and include combustion of fossil fuels, industry outfalls, emissions from internal combustion engines, forest fires, and volcanic activity (Eisler, 1987, Neff, 1979). Petrogenic PAHs (2 to 3 rings) are derived at low temperatures (~ 150 °C), under high pressure, over geological time (Neff, 1979), and lead to the formation of fossil fuels. Petrogenic PAHs are usually associated with localized sources (Burgess et al., 2003), are typically found at background concentrations (Gschwend et al., 1983), and are characterized by their acute toxicity to aquatic organisms (Eisler, 1987, Neff, 1979). Polycyclic aromatic hydrocarbons are a major environmental concern due to their carcinogenic and mutagenic effects, their ubiquitous distribution in aquatic systems, and their hydrophobic properties that result in high sediment concentrations (Eisler, 1987, Neff, 1979). Studies have found that PAHs at extremely low concentrations (5 to 70 ppt) are toxic to many organisms including zooplankton and fish (Giesy et al., 1983, Juttner et al., 1995). A recent historical overview of Great Lakes contaminants found a close association between concentrations of PAHs in sediments and hepatic neoplasia in brown bullhead (Rafferty et al., 2009).

There is a strong positive correlation between the degree of urbanization and the concentration of PAHs in sediments (Buehler et al., 2001, Neff, 1979). Most research on PAHs in sediments has been conducted in heavily contaminated urban and industrialized areas, including wastewater treatment outfalls, storm-water discharges, coking facilities, petroleum depots, and coal storage sites (e.g., Ashley and Baker, 1999, Carr et al., 2000, Crane et al., 1997, Kemble et al., 2000; Zeng and Vista, 1997). Assessing ecological effects of contaminated sediments in these areas is relatively straightforward. While elevated PAHs have been associated with marinas, harbors, fuel docks, and boating activities in heavily populated and highly developed areas (Albers, 2002, Fang et al., 2003), few studies have investigated impacts of PAHs at remote locations.

This two-year study used the sediment quality triad (SQT) (Chapman, 1986, Long and Chapman, 1985) to evaluate effects of PAHs in sediments on benthic macroinvertebrate communities in Isle Royale National Park, USA. SQT is an approach used to determine the correlation between the bioavailability of mixtures of chemical contaminants in sediments and biological effects (Chapman, 1990). This methodology combines observations of sediment chemistry, benthic community structure, and sediment toxicity to evaluate sediment quality. Sediment quality is determined by combining the response from each assessment to build a weight-of-evidence (WOE). Weight-of-evidence approaches have been classified into three categories, metaphorical, methodological, and theoretical (Weed, 2005). Methodological WOE approaches are often used in environmental risk assessments (Weed, 2005). Integration of the evidence can vary from listing evidence to a formal process of decision analysis and statistical methods (Linkov et al., 2009).

The objectives of the study were to: i) determine the spatial distribution of PAHs in sediments collected from marinas and nearby reference sites; ii) assess potential effects of PAHs on benthic macroinvertebrate communities; iii) measure the toxicity of PAHs to macroinvertebrates in whole sediments; and iv) quantify bioaccumulation of PAHs in the burrowing mayfly Hexagenia limbata.

Section snippets

Study area

Isle Royale National Park is located on a large (535 km2) remote island in the western basin of Lake Superior. Visitation to the Park is limited, occurring between April and October with approximately 17,000 visitors per year. In contrast, Yellowstone National Park is visited by 3 million people annually. Because we lacked information on PAH concentrations in sediments, sample locations in the Park were identified based on motorboat activity. Motorboats have been documented as a substantial

Site characterization

Routine physicochemical characteristics that we measured were similar among sites and showed little differences between marinas and reference areas with the exception of total organic carbon (Table 2). Mean percent TOC in sediment was variable (0.08% to 2.39%) but was greater at each marina sites compared to the paired reference site, although there was overlap in the ranges observed. Mean depth was also variable among sites, ranging from 1.8 to 10.8 m. Mean conductivity ranged from 84.6 μS to

Discussion

Although concentrations of PAHs and other legacy contaminants are generally lower in Lake Superior compared to the other Great Lakes (Gschwend and Hites, 1981), elevated levels of these contaminants do occur in developed areas. Consistent with research conducted in marine ecosystems (Johnson et al., 1985), PAH concentrations in surface sediments were greatly elevated at marinas compared to reference and background sites. The highest PAH concentrations were measured at Rock Harbor marina, and

Conclusions

The observed patterns of increased PAH contamination in sediments, decreased survival of H. azteca, reduced abundance of Diporeia spp. and bioaccumulation of PAHs by H. limbata suggested moderate impairment of benthic communities in marinas at Isle Royale National Park. Levels of PAHs measured in the mayfly H. limbata demonstrated that some constituents, especially low molecular weight compounds, were bioavailable to macroinvertebrates. Measuring the effects of PAHs on benthic communities in

Acknowledgments

We thank Guy Denoux, Donna Kashian, Katy Mitchell, Travis Schmidt, and Bob Zuellig for input and support throughout this project. We are especially grateful to Jean Battle, Alex Egan, Roy Irwin, Brenda Moraska-Lafrancois, and Mark Romanski at the U.S. National Park Service for logistical support and other contributions. Daren Carlisle at the U.S. Geological Survey was instrumental in initiating this work. Funding for this project was provided by the U.S. National Park Service.

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