Johanna M. Kraus

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.

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.

Metamorphosis alters contaminants and chemical tracers in insects: implications for food webs.

Insects are integral to most freshwater and terrestrial food webs, but due to their accumulation of environmental pollutants they are also contaminant vectors that threaten reproduction, development, and survival of consumers. Metamorphosis from larvae to adult can cause large chemical changes in insects, altering contaminant concentrations and fractionation of chemical tracers used to establish contaminant biomagnification in food webs, but no framework exists for predicting and managing these effects. We analyzed data from 39 studies of 68 analytes (stable isotopes and contaminants), and found that metamorphosis effects varied greatly. δ(15)N, widely used to estimate relative trophic position in biomagnification studies, was enriched by ∼ 1‰ during metamorphosis, while δ(13)C used to estimate diet, was similar in larvae and adults. Metals and polycyclic aromatic hydrocarbons (PAHs) were predominantly lost during metamorphosis leading to ∼ 2 to 125-fold higher larval concentrations and higher exposure risks for predators of larvae compared to predators of adults. In contrast, manufactured organic contaminants (such as polychlorinated biphenyls) were retained and concentrated in adults, causing up to ∼ 3-fold higher adult concentrations and higher exposure risks to predators of adult insects. Both food web studies and contaminant management and mitigation strategies need to consider how metamorphosis affects the movement of materials between habitats and ecosystems, with special regard for aquatic-terrestrial linkages.

Riparian spiders as sentinels of polychlorinated biphenyl contamination across heterogeneous aquatic ecosystems

Riparian spiders are being used increasingly to track spatial patterns of contaminants in and fluxing from aquatic ecosystems. However, our understanding of the circumstances under which spiders are effective sentinels of aquatic pollution is limited. The present study tests the hypothesis that riparian spiders may be effectively used to track spatial patterns of sediment pollution by polychlorinated biphenyls (PCBs) in aquatic ecosystems with high habitat heterogeneity. The spatial pattern of ΣPCB concentrations in 2 common families of riparian spiders sampled in 2011 to 2013 generally tracked spatial variation in sediment ΣPCBs across all sites within the Manistique River Great Lakes Area of Concern (AOC), a rivermouth ecosystem located on the south shore of the Upper Peninsula, Manistique (MI, USA) that includes harbor, river, backwater, and lake habitats. Sediment ΣPCB concentrations normalized for total organic carbon explained 41% of the variation in lipid-normalized spider ΣPCB concentrations across 11 sites. Furthermore, 2 common riparian spider taxa (Araneidae and Tetragnathidae) were highly correlated (r2  > 0.78) and had similar mean ΣPCB concentrations when averaged across all years. The results indicate that riparian spiders may be useful sentinels of relative PCB availability to aquatic and riparian food webs in heterogeneous aquatic ecosystems like rivermouths where habitat and contaminant variability may make the use of aquatic taxa less effective. Furthermore, the present approach appears robust to heterogeneity in shoreline development and riparian vegetation that support different families of large web-building spiders. Environ Toxicol Chem 2017;36:1278-1286. Published 2016 Wiley Periodicals, Inc. on behalf of SETAC. This article is a US government work and, as such, is in the public domain in the United States of America.

Metamorphosis Affects Metal Concentrations and Isotopic Signatures in a Mayfly (Baetis tricaudatus): Implications for the Aquatic-Terrestrial Transfer of Metals

Insect metamorphosis often results in substantial chemical changes that can alter contaminant concentrations and fractionate isotopes. We exposed larval mayflies (Baetis tricaudatus) and their food (periphyton) to an aqueous zinc gradient (3-340 μg Zn/l) and measured zinc concentrations at different stages of metamorphosis: larval, subimago, and imago. We also measured changes in stable isotopes (δ15N and δ13C) in unexposed mayflies. Larval zinc concentrations were positively related to aqueous zinc, increasing 9-fold across the exposure gradient. Adult zinc concentrations were also positively related to aqueous zinc, but were 7-fold lower than larvae. This relationship varied according to adult substage and sex. Tissue concentrations in female imagoes were not related to exposure concentrations, but the converse was true for all other stage-by-sex combinations. Metamorphosis also increased δ15N by ∼0.8‰, but not δ13C. Thus, the main effects of metamorphosis on insect chemistry were large declines in zinc concentrations coupled with increased δ15N signatures. For zinc, this change was largely consistent across the aqueous exposure gradient. However, differences among sexes and stages suggest that caution is warranted when using nitrogen isotopes or metal concentrations measured in one insect stage (e.g., larvae) to assess risk to wildlife that feed on subsequent life stages (e.g., adults).

Low-cost floating emergence net and bottle trap: comparison of two designs

ABSTRACT Sampling emergent aquatic insects is of interest to many freshwater ecologists. Many quantitative emergence traps require the use of aspiration for collection. However, aspiration is infeasible in studies with large amounts of replication that is often required in large biomonitoring projects. We designed an economic, collapsible pyramid-shaped floating emergence trap with an external collection bottle that avoids the need for aspiration. This design was compared experimentally to a design of similar dimensions that relied on aspiration to ensure comparable results. The pyramid-shaped design captured twice as many total emerging insects. When a preservative was used in bottle collectors, >95% of the emergent abundance was collected in the bottle. When no preservative was used, >81% of the total insects were collected from the bottle. In addition to capturing fewer emergent insects, the traps that required aspiration took significantly longer to sample. Large studies and studies sampling remote locations could benefit from the economical construction, speed of sampling, and capture efficiency.

A modeling approach to compare ΣPCB concentrations between congener-specific analyses.

Changes in analytical methods over time pose problems for assessing long-term trends in environmental contamination by PCBs. Congener-specific analyses vary widely in the number and identity of the 209 distinct PCB chemical configurations (congeners) that are quantified, leading to inconsistencies among summed PCB concentrations (ΣPCB) reported by different studies. Here, we present a modeling approach using linear regression to compare ΣPCB concentrations derived from different congener-specific analyses measuring different co-eluting groups. The approach can be used to develop a specific conversion model between any 2 sets of congener-specific analytical data from similar samples (similar matrix and geographic origin). We demonstrate the method by developing a conversion model for an example data set that includes data from 2 different analytical methods, a low resolution method quantifying 119 congeners and a high resolution method quantifying all 209 congeners. We used the model to show that the 119-congener set captured most (93%) of the total PCB concentration (i.e., Σ209 PCB) in sediment and biological samples. ΣPCB concentrations estimated using the model closely matched measured values (mean relative percent difference = 9.6). General applications of the modeling approach include 1) generating comparable ΣPCB concentrations for samples that were analyzed for different congener sets; and 2) estimating the proportional contribution of different congener sets to ΣPCB. This approach may be especially valuable for enabling comparison of long-term remediation monitoring results even as analytical methods change over time. Integr Environ Assess Manag 2017;13:227-232. Published 2016. This article is a U.S. Government work and is in the public domain in the USA.

Riparian spiders as sentinels of PCB contamination across heterogeneous aquatic ecosystems

Riparian spiders are being used increasingly to track spatial patterns of contaminants in and fluxing from aquatic ecosystems. However, our understanding of the circumstances under which spiders are effective sentinels of aquatic pollution is limited. The present study tests the hypothesis that riparian spiders may be effectively used to track spatial patterns of sediment pollution by polychlorinated biphenyls (PCBs) in aquatic ecosystems with high habitat heterogeneity. The spatial pattern of ΣPCB concentrations in 2 common families of riparian spiders sampled in 2011 to 2013 generally tracked spatial variation in sediment ΣPCBs across all sites within the Manistique River Great Lakes Area of Concern (AOC), a rivermouth ecosystem located on the south shore of the Upper Peninsula, Manistique (MI, USA) that includes harbor, river, backwater, and lake habitats. Sediment ΣPCB concentrations normalized for total organic carbon explained 41% of the variation in lipid-normalized spider ΣPCB concentrations across 11 sites. Furthermore, 2 common riparian spider taxa (Araneidae and Tetragnathidae) were highly correlated (r2  > 0.78) and had similar mean ΣPCB concentrations when averaged across all years. The results indicate that riparian spiders may be useful sentinels of relative PCB availability to aquatic and riparian food webs in heterogeneous aquatic ecosystems like rivermouths where habitat and contaminant variability may make the use of aquatic taxa less effective. Furthermore, the present approach appears robust to heterogeneity in shoreline development and riparian vegetation that support different families of large web-building spiders. Environ Toxicol Chem 2017;36:1278-1286. Published 2016 Wiley Periodicals, Inc. on behalf of SETAC. This article is a US government work and, as such, is in the public domain in the United States of America.

In vivo isotopic fractionation of zinc and biodynamic modeling yield insights into detoxification mechanisms in the mayfly Neocloeon triangulifer

Diversity and biomass of aquatic insects decline in metal-rich aquatic environments, but the mechanisms by which insects from such environments cope with potentially toxic metal concentrations to survive through adulthood are less well understood. In this study, we measured Zn concentrations and isotopes in laboratory-reared diatoms and mayflies (Neocloeon triangulifer) from larval through adult stages. The larvae were fed Zn-enriched diatoms, and bio-concentrated Zn by a factor of 2.5-5 relative to the diatoms but maintained the same Zn-isotopic ratio. These results reflect the importance of dietary uptake and the greater rate of uptake relative to excretion or growth. Upon metamorphosis to subimago, Zn concentrations declined by >70%, but isotopically heavy Zn remained in the subimago bodies. We surmised that the loss of isotopically light Zn during metamorphosis was due to the loss of detoxified Zn and retention of metabolically useful Zn. Through the transition from subimago to imago, Zn concentrations and isotope ratios were virtually unchanged. Because the decrease in Zn body concentration and increase in heavier Zn are seen in the subimagos relative to the larvae, the compartmentalization of Zn must be occurring within the larvae. A biodynamic model was constructed, allowing for isotopic fractionation and partitioning of Zn between metabolically essential and detoxified Zn reservoirs within larvae. The model provides a consistent set of rate and fractionation constants that successfully describe the experimental observations. Specifically, metabolically essential Zn is isotopically heavier and is tightly held once assimilated, and excess, isotopically light Zn is sequestered, detoxified, and ultimately lost during the metamorphosis of larvae to subimagos. To our knowledge, this is the first documentation of in vivo isotopic fractionation in insects, offering an improved understanding of the mechanisms and rates by which the N. triangulifer larvae regulate excess Zn in their bodies.