David M. Walters

THE DARK SIDE OF SUBSIDIES: ADULT STREAM INSECTS EXPORT ORGANIC CONTAMINANTS TO RIPARIAN PREDATORS

Aquatic insects provide a critical energy subsidy to riparian food webs, yet their role as vectors of contaminants to terrestrial ecosystems is poorly understood. We investigated relationships between aquatic resource utilization and contaminant exposure for a riparian invertivore assemblage (spiders and herptiles) along a stream contaminated with polychlorinated biphenyls (PCBs). Stable carbon (delta13C) and nitrogen (delta15N) isotopes indicated that aquatic insect utilization varied among predators, with progressive enrichment of delta13C and depletion of delta15N as predators shifted from aquatic to terrestrial prey. PCB concentrations significantly increased along these isotopic gradients; delta13C and delta15N explained 65% and 15% of the variance in predator sigmaPCBs, respectively. PCBs in predators were high, exceeding 2000 ng/g wet mass (the human-health advisory prohibiting any consumption of fish tissue) in three species. Greater consideration should be given to streams as lateral exporters rather than simply as longitudinal conduits for contaminants. Persistent contaminants are underutilized for addressing landscape-level questions in subsidy research, but our results demonstrate they are an ideal in situ tracer of stream-derived energy because they label stream organic matter and invertebrates over large distances. Likewise, riparian predators such as tetragnathid spiders have great potential as biological monitors of stream condition and as an assessment tool for risk management of contaminated aquatic sediments.

Spider-mediated flux of PCBs from contaminated sediments to terrestrial ecosystems and potential risks to arachnivorous birds

We investigated aquatic insect utilization and PCB exposure in riparian spiders at the Lake Hartwell Superfund site (Clemson, SC). We sampled sediments, adult chironomids, terrestrial insects, riparian spiders (Tetragnathidae, Araneidae, and Mecynogea lemniscata), and upland spiders (Araneidae) along a sediment contamination gradient. Stable isotopes (delta(13)C, delta(15)N) indicated that riparian spiders primarily consumed aquatic insects whereas upland spiders consumed terrestrial insects. PCBs in chironomids (mean 1240 ng/g among sites) were 2 orders of magnitude higher than terrestrial insects (15.2 ng/g), similar to differences between riparian (820-2012 ng/g) and upland spiders (30 ng/g). Riparian spider PCBs were positively correlated with sediment concentrations for all taxa (r(2) = 0.44-0.87). We calculated spider-based wildlife values (WVs, the minimum spider PCB concentrations causing physiologically significant doses in consumers) to assess exposure risks for arachnivorous birds. Spider concentrations exceeded WVs for most birds at heavily contaminated sites and were approximately 14-fold higher for the most sensitive species (chickadee nestlings, Poecile spp.). Spiders are abundant and ubiquitous in riparian habitats, where they depend on aquatic insect prey. These traits, along with the high degree of spatial correlation between spider and sediment concentrations we observed, suggest that they are model indicator species for monitoring contaminated sediment sites and assessing risks associated with contaminant flux into terrestrial ecosystems.

Physical indicators of hydrologic permanence in forested headwater streams

Abstract Recent court cases have questioned whether all headwater streams are jurisdictional waters under the US Clean Water Act. Rapid field-based indicators of hydrologic permanence are needed for making jurisdictional determinations. Our study objectives were to: 1) identify physical characteristics of forested headwater streams that best distinguish perennial, intermittent, and ephemeral reaches and 2) assess the applicability of existing rapid field-based tools for classifying hydrologic permanence across a wide geographic range. We surveyed reach- and drainage-scale characteristics at 113 sites across 10 study forests in the US. Streams in 4 core forests (61 core sites) were sampled over 2 consecutive years and were used in model construction. Streams in 6 satellite forests (72 satellite sites) were used to validate the models over a broader geographic range. Discriminant function models successfully differentiated hydrologic permanence categories at core sites. Drainage area, the Ohio Environmental Protection Agency Headwater Habitat Evaluation Index (HHEI), and the North Carolina Department of Water Quality Stream Classification Method (NCSC) were strongly correlated with the discriminant function that separated ephemeral from perennial and intermittent sites. Entrenchment ratio was the most consistent variable discriminating intermittent from perennial sites across the core forests. The models had mixed results when applied to the validation data set, but did classify correctly most intermittent and ephemeral sites. Classification trees were used to assess broad regional applicability of existing rapid field-based protocols and to identify important metrics. Scores from the Rapid Bioassessment Protocol Habitat Assessment, HHEI, and NCSC all clearly distinguished ephemeral from intermittent and perennial sites, but no differences were detected between intermittent and perennial sites across all sites. However, data from core sites do indicate that a suite of physical variables can be used successfully to identify hydrologic permanence at regional scales.

Trophic magnification of PCBs and its relationship to the octanol-water partition coefficient

We investigated polychlorinated biphenyl (PCB) bioaccumulation relative to octanol-water partition coefficient (K(OW)) and organism trophic position (TP) at the Lake Hartwell Superfund site (South Carolina). We measured PCBs (127 congeners) and stable isotopes (δ¹⁵N) in sediment, organic matter, phytoplankton, zooplankton, macroinvertebrates, and fish. TP, as calculated from δ¹⁵N, was significantly, positively related to PCB concentrations, and food web trophic magnification factors (TMFs) ranged from 1.5-6.6 among congeners. TMFs of individual congeners increased strongly with log K(OW), as did the predictive power (r²) of individual TP-PCB regression models used to calculate TMFs. We developed log K(OW)-TMF models for eight food webs with vastly different environments (freshwater, marine, arctic, temperate) and species composition (cold- vs warmblooded consumers). The effect of K(OW) on congener TMFs varied strongly across food webs (model slopes 0.0-15.0) because the range of TMFs among studies was also highly variable. We standardized TMFs within studies to mean = 0, standard deviation (SD) = 1 to normalize for scale differences and found a remarkably consistent K(OW) effect on TMFs (no difference in model slopes among food webs). Our findings underscore the importance of hydrophobicity (as characterized by K(OW)) in regulating bioaccumulation of recalcitrant compounds in aquatic systems, and demonstrate that relationships between chemical K(OW) and bioaccumulation from field studies are more generalized than previously recognized.

Persistent organic pollutants in fish tissue in the mid-continental great rivers of the United States

Great rivers of the central United States (Upper Mississippi, Missouri, and Ohio rivers) are valuable economic and cultural resources, yet until recently their ecological condition has not been well quantified. In 2004-2005, as part of the Environmental Monitoring and Assessment Program for Great River Ecosystems (EMAP-GRE), we measured legacy organochlorines (OCs) (pesticides and polychlorinated biphenyls, PCBs) and emerging compounds (polybrominated diphenyl ethers, PBDEs) in whole fish to estimate human and wildlife exposure risks from fish consumption. PCBs, PBDEs, chlordane, dieldrin and dichlorodiphenyltrichloroethane (DDT) were detected in most samples across all rivers, and hexachlorobenzene was detected in most Ohio River samples. Concentrations were highest in the Ohio River, followed by the Mississippi and Missouri Rivers, respectively. Dieldrin and PCBs posed the greatest risk to humans. Their concentrations exceeded human screening values for cancer risk in 27-54% and 16-98% of river km, respectively. Chlordane exceeded wildlife risk values for kingfisher in 11-96% of river km. PBDE concentrations were highest in large fish in the Missouri and Ohio Rivers (mean>1000 ng g(-1) lipid), with congener 47 most prevalent. OC and PBDE concentrations were positively related to fish size, lipid content, trophic guild, and proximity to urban areas. Contamination of fishes by OCs is widespread among great rivers, although exposure risks appear to be more localized and limited in scope. As an indicator of ecological condition, fish tissue contamination contributes to the overall assessment of great river ecosystems in the U.S.

The distance that contaminated aquatic subsidies extend into lake riparian zones

Consumption of emergent aquatic insects by terrestrial invertebrates is a poorly resolved, but potentially important, mechanism of contaminant flux across ecosystem borders leading to contaminant exposure in terrestrial invertivores. We characterized the spatial extent and magnitude of contaminant transfer from aquatic sediments to terrestrial invertebrate predators by examining riparian araneid spiders, terrestrial insects, and emergent aquatic insects for stable isotopes and polychlorinated biphenyls (PCBs, sum of 141 congeners) at Lake Hartwell, (Clemson, South Carolina, USA). PCB concentrations in aquatic insects were orders of magnitude higher than in terrestrial insects. Aquatic insect consumption by spiders (as indicated by delta13C and delta15N), PCB concentrations in spiders, and aquatic prey availability were greatest at the shoreline and declined inland, while terrestrial prey availability was invariant with distance. These patterns indicate PCB transfer to spiders through consumption of emergent aquatic insects extending to a distance of 5 m inland. Measurable, but much lower, PCBs were present in insect predators dominated by social wasps up to 30 m inland. These results illustrate the importance of emergent insects as vectors of contaminant transfer from lake sediments to riparian food webs, and that spiders are key predators in this process.

Cross-ecosystem impacts of stream pollution reduce resource and contaminant flux to riparian food webs

The effects of aquatic contaminants are propagated across ecosystem boundaries by aquatic insects that export resources and contaminants to terrestrial food webs; however, the mechanisms driving these effects are poorly understood. We examined how emergence, contaminant concentration, and total contaminant flux by adult aquatic insects changed over a gradient of bioavailable metals in streams and how these changes affected riparian web-building spiders. Insect emergence decreased 97% over the metal gradient, whereas metal concentrations in adult insects changed relatively little. As a result, total metal exported by insects (flux) was lowest at the most contaminated streams, declining 96% among sites. Spiders were affected by the decrease in prey biomass, but not by metal exposure or metal flux to land in aquatic prey. Aquatic insects are increasingly thought to increase exposure of terrestrial consumers to aquatic contaminants, but stream metals reduce contaminant flux to riparian consumers by strongly impacting the resource linkage. Our results demonstrate the importance of understanding the contaminant-specific effects of aquatic pollutants on adult insect emergence and contaminant accumulation in adults to predict impacts on terrestrial food webs.

Emergence flux declines disproportionately to larval density along a stream metals gradient

Effects of contaminants on adult aquatic insect emergence are less well understood than effects on insect larvae. We compared responses of larval density and adult emergence along a metal contamination gradient. Nonlinear threshold responses were generally observed for larvae and emergers. Larval densities decreased significantly at low metal concentrations but precipitously at concentrations of metal mixtures above aquatic life criteria (cumulative criterion accumulation ratio (CCAR) ≥ 1). In contrast, adult emergence declined precipitously at low metal concentrations (CCAR ≤ 1), followed by a modest decline above this threshold. Adult emergence was a more sensitive indicator of the effect of low metals concentrations on aquatic insect communities compared to larvae, presumably because emergence is limited by a combination of larval survival and other factors limiting successful emergence. Thus effects of exposure to larvae are not manifest until later in life (during metamorphosis and emergence). This loss in emergence reduces prey subsidies to riparian communities at concentrations considered safe for aquatic life. Our results also challenge the widely held assumption that adult emergence is a constant proportion of larval densities in all streams.

Genetic diversity and species diversity of stream fishes covary across a land-use gradient

Genetic diversity and species diversity are expected to covary according to area and isolation, but may not always covary with environmental heterogeneity. In this study, we examined how patterns of genetic and species diversity in stream fishes correspond to local and regional environmental conditions. To do so, we compared population size, genetic diversity and divergence in central stonerollers (Campostoma anomalum) to measures of species diversity and turnover in stream fish assemblages among similarly sized watersheds across an agriculture–forest land-use gradient in the Little Miami River basin (Ohio, USA). Significant correlations were found in many, but not all, pair-wise comparisons. Allelic richness and species richness were strongly correlated, for example, but diversity measures based on allele frequencies and assemblage structure were not. In-stream conditions related to agricultural land use were identified as significant predictors of genetic diversity and species diversity. Comparisons to population size indicate, however, that genetic diversity and species diversity are not necessarily independent and that variation also corresponds to watershed location and glaciation history in the drainage basin. Our findings demonstrate that genetic diversity and species diversity can covary in stream fish assemblages, and illustrate the potential importance of scaling observations to capture responses to hierarchical environmental variation. More comparisons according to life history variation could further improve understanding of conditions that give rise to parallel variation in genetic diversity and species diversity, which in turn could improve diagnosis of anthropogenic influences on aquatic ecosystems.

Metamorphosis Enhances the Effects of Metal Exposure on the Mayfly, Centroptilum triangulifer

The response of larval aquatic insects to stressors such as metals is used to assess the ecological condition of streams worldwide. However, nearly all larval insects metamorphose from aquatic larvae to winged adults, and recent surveys indicate that adults may be a more sensitive indicator of stream metal toxicity than larvae. One hypothesis to explain this pattern is that insects exposed to elevated metal in their larval stages have a reduced ability to successfully complete metamorphosis. To test this hypothesis we exposed late-instar larvae of the mayfly, Centroptilum triangulifer, to an aqueous Zn gradient (32-476 μg/L) in the laboratory. After 6 days of exposure, when metamorphosis began, larval survival was unaffected by zinc. However, Zn reduced wingpad development at concentrations above 139 μg/L. In contrast, emergence of subimagos and imagos tended to decline with any increase in Zn. At Zn concentrations below 105 μg/L (hardness-adjusted aquatic life criterion), survival between the wingpad and subimago stages declined 5-fold across the Zn gradient. These results support the hypothesis that metamorphosis may be a survival bottleneck, particularly in contaminated streams. Thus, death during metamorphosis may be a key mechanism explaining how stream metal contamination can impact terrestrial communities by reducing aquatic insect emergence.