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Critical tissue residue approach linking accumulated metals in aquatic insects to population and community-level effects

Whole body Zn concentrations in individuals ( n = 825) from three aquatic insect taxa (mayflies Rhithrogena spp. and Drunella spp. and the caddisfly Arctopsyche grandis ) were used to predict effects on populations and communities ( n = 149 samples). Both mayflies accumulated significantly more Zn than the caddisfly. The presence/absence of Drunella spp. most reliably distinguished sites with low and high Zn concentrations; however, population densities of mayflies were more sensitive to increases in accumulated Zn. Critical tissue residues (634 μg/g Zn for Drunella spp. and 267 μg/g Zn for Rhithrogena spp.) caused a 20% reduction in maximum (90th quantile) mayfly densities. These critical tissue residues were associated with exposure to 7.0 and 3.9 μg/L dissolved Zn for Drunella spp. and Rhithrogena spp., respectively. A threshold in a measure of taxonomic completeness (observed/expected) was observed at 5.4 μg/L dissolved Zn. Dissolved Zn concentrations associated with critical tissue residues in mayflies were also associated with adverse effects in the aquatic community as a whole. These effects on populations and communities occurred at Zn concentrations below the U.S. EPA hardness-adjusted continuous chronic criterion.

Environmental Science & Technology

Copper, cadmium, and zinc concentrations in juvenile Chinook salmon and selected fish-forage organisms (aquatic insects) in the upper Sacramento River, California

This study assessed the downstream extent andseverity of copper (Cu), cadmium (Cd), and zinc (Zn)contamination from acid mine drainage on juvenile chinook salmon( Oncorhynchus tshawytscha ) and aquatic insects over aroughly 270-km reach of the Sacramento River below KeswickReservoir. During April–May 1998, salmon were collected fromfour sites in the river and from a fish hatchery that receiveswater from Battle Creek. Salmon from river sites were examinedfor gut contents to document their consumption of variousinvertebrate taxa, whereas salmon from river sites and thehatchery were used for metal determinations. Midge(Chironomidae) and caddisfly (Trichoptera) larvae and mayfly(Ephemeroptera) nymphs were collected for metal determinationsduring April–June from river sites and from Battle and Buttecreeks. The fish hatchery and Battle and Butte creeks served asreference sites because they had no history of receiving minedrainage. Salmon consumed mostly midge larvae and pupae (44.0%,damp-dry biomass), caddisfly larvae (18.9%), Cladocera (5.8%),and mayfly nymphs (5.7%). These results demonstrated thatinsects selected for metal determinations were important as fishforage. Dry-weight concentrations of Cu, Cd, and Zn weregenerally far higher in salmon and insects from the river thanfrom reference sites. Within the river, high metalconcentrations persisted as far downstream as South Meridian (thelowermost sampling site). Maximum concentrations of Cd (30.7 μg g -1 ) and Zn (1230 μg g -1 ),but not Cu (87.4 μg g -1 ), in insects exceeded amounts that other investigators reported as toxic when fed for prolonged periods to juvenile salmonids.

California

Aquatic insect accumulation of uranium at spring outflows in the Grand Canyon region as influenced by aqueous and sediment geochemistry and biological factors: Implications for monitoring

Potential adverse ecological effects of expanded uranium (U) mining within the Grand Canyon region motivated studies to better understand U exposure and risk to endemic species. This study documents U exposures and analyzes geochemical and biological factors affecting U bioaccumulation at spring-fed systems within the Grand Canyon region. The principal objective was to determine if aqueous U was broadly indicative of U accumulated by insect larvae, a dominate fauna. Analyses focused on three widely distributed taxa: Argia sp. (a predatory damselfly), Culicidae (suspension feeding mosquitos), and Limnephilus sp. (a detritivorous caddisfly). The study showed that U accumulated by aquatic insects (and periphyton) generally correlated positively with total dissolved U, although correlations were strongest when based on modeled concentrations of the U-dicarbonato complex, UO 2 (CO 3 ) 2 –2 , and UO 2 (OH) 2 . Sediment metal concentration was a redundant indicator of U bioaccumulation. Neither insect size or U in the gut content of Limnephilus sp. substantially affected correlations between aqueous U and whole-body U concentrations. However, in Limnephilus sp., the gut and its content contained large quantities of U. Estimates of the sediment burden in the gut indicated that sediment was a minor source of U mass but contributed substantially to the total insect weight. As a result, whole-body U concentration would tend to vary inversely with the sediment burden of the gut. The correlations between aqueous U and bioaccumulated U provide an initial relational baseline against which newly acquired data could be evaluated for changes in U exposure during and after mining operations.

Arizona

Aquatic insect ecophysiological traits reveal phylogenetically based differences in dissolved cadmium susceptibility

We used a phylogenetically based comparative approach to evaluate the potential for physiological studies to reveal patterns of diversity in traits related to susceptibility to an environmental stressor, the trace metal cadmium (Cd). Physiological traits related to Cd bioaccumulation, compartmentalization, and ultimately susceptibility were measured in 21 aquatic insect species representing the orders Ephemeroptera, Plecoptera, and Trichoptera. We mapped these experimentally derived physiological traits onto a phylogeny and quantified the tendency for related species to be similar (phylogenetic signal). All traits related to Cd bioaccumulation and susceptibility exhibited statistically significant phylogenetic signal, although the signal strength varied among traits. Conventional and phylogenetically based regression models were compared, revealing great variability within orders but consistent, strong differences among insect families. Uptake and elimination rate constants were positively correlated among species, but only when effects of body size and phylogeny were incorporated in the analysis. Together, uptake and elimination rates predicted dramatic Cd bioaccumulation differences among species that agreed with field-based measurements. We discovered a potential tradeoff between the ability to eliminate Cd and the ability to detoxify it across species, particularly mayflies. The best-fit regression models were driven by phylogenetic parameters (especially differences among families) rather than functional traits, suggesting that it may eventually be possible to predict a taxon's physiological performance based on its phylogenetic position, provided adequate physiological information is available for close relatives. There appears to be great potential for evolutionary physiological approaches to augment our understanding of insect responses to environmental stressors in nature. ?? 2008 by The National Academy of Sciences of the USA.

Proceedings of the National Academy of Sciences of

Larval aquatic insect responses to cadmium and zinc in experimental streams

To evaluate the risks of metal mixture effects to natural stream communities under ecologically relevant conditions, the authors conducted 30-d tests with benthic macroinvertebrates exposed to cadmium (Cd) and zinc (Zn) in experimental streams. The simultaneous exposures were with Cd and Zn singly and with Cd+Zn mixtures at environmentally relevant ratios. The tests produced concentration–response patterns that for individual taxa were interpreted in the same manner as classic single-species toxicity tests and for community metrics such as taxa richness and mayfly (Ephemeroptera) abundance were interpreted in the same manner as with stream survey data. Effect concentrations from the experimental stream exposures were usually 2 to 3 orders of magnitude lower than those from classic single-species tests. Relative to a response addition model, which assumes that the joint toxicity of the mixtures can be predicted from the product of their responses to individual toxicants, the Cd+Zn mixtures generally showed slightly less than additive toxicity. The authors applied a modeling approach called Tox to explore the mixture toxicity results and to relate the experimental stream results to field data. The approach predicts the accumulation of toxicants (hydrogen, Cd, and Zn) on organisms using a 2-p K a bidentate model that defines interactions between dissolved cations and biological receptors (biotic ligands) and relates that accumulation through a logistic equation to biological response. The Tox modeling was able to predict Cd+Zn mixture responses from the single-metal exposures as well as responses from field data. The similarity of response patterns between the 30-d experimental stream tests and field data supports the environmental relevance of testing aquatic insects in experimental streams.

Environmental Toxicology and Chemistry

Can activity traps assess aquatic insect abundance at the landscape level?

We used activity traps as designed by Riley and Bookhout (1990. Wetlands) to sample aquatic invertebrates as part of a study to characterize wetlands on a forested and an agricultural landscape (ca. 1,000 mi'2) in northern. Maine. Eight wetlands (5 from agricultural and 3 from forested landscapes) were sampled at random from 50 wetlands surveyed for waterfowl broods. At the landscape level, insect abundance (mean no./ trap), fish abundance (mean no./trap), percent vegetation, and water chemistry variables (pH, ANC, SPCOND, Ca, Mg, K, Na, Cl) were different between landscapes. Furthermore, nearly as many fish (2,112) were caught as were insects (2,443); 47% of the 332 traps contained fish, but 84 traps accounted for 94% of the fish caught. When >4 fish were in a trap fewer insects were in the trap. Differences in water temperature among wetlands and differences in rates of escape among insect orders affected the number of different taxa caught. Until capture success of activity traps is better understood, results from activity traps should be used with care.

Bulletin of the North American Benthological Socie

Spatial population structure of a widespread aquatic insect in the Colorado River Basin: Evidence for a Hydropsyche oslari species complex

Structural connectivity and dispersal ability are important constraints on functional connectivity among populations. For aquatic organisms that disperse among stream corridors, the regional structure of a river network can, thus, define the boundaries of gene flow. In this study, we used mitochondrial DNA (mtCO1 barcoding gene) to examine the genetic diversity and population structure of a caddisfly with strong dispersal capabilities, Hydropsyche oslari (Trichoptera:Hydropsychidae), in the topologically-diverse Colorado River Basin. We expected to find less genetic differentiation among populations of H . oslari within the Upper Basin, which has a dense dendritic network of perennial tributaries that allow for greater potential dispersal and gene flow, than among populations within the arid and sparse river network of the Lower Basin. We also expected to find genetic differentiation among H. oslari in the Upper and Lower Basins because contemporary populations are geographically distant from each other and have been separated by a >300-km-long reservoir (Lake Powell) for ½ a century. Consistent with these predictions, we found that populations of H . oslari within the Upper Basin had more shared haplotypes and less nucleotide diversity (π = 0.001–0.008) than H . oslari within the Lower Basin ( F ST = 0.01, π = 0.014–0.028). However, populations were genetically more structured in the Upper Basin ( F ST = 0.47) than in the Lower Basin ( F ST = 0.01). We also found that populations in the Upper and Lower Basin are entirely genetically differentiated ( S nn = 1), suggesting that these 2 populations were isolated thousands of years before the 1963 closure of Glen Canyon Dam and subsequent filling of Lake Powell. The most similar haplotypes among the 2 basins represent a 5.4% difference, which indicates the presence of a species complex within H. oslari .

Colorado River Basin

Measured efficacy, bioaccumulation, and leaching of a transfluthrin-based insecticidal paint: A case study with a nuisance, nonbiting aquatic insect

BACKGROUND Pest management professionals will require a diverse, adaptive abatement toolbox to combat advanced challenges from disease vector and nuisance insect populations. Designed for post-application longevity, insecticidal paints offer extended residual effects on targeted insect pest populations; a measured understanding of active ingredient bioavailability over time is valuable to fully assess treatment efficacy and potential environmental risks. This study was initiated because a nuisance net-spinning caddisfly, Smicridea fasciatella , is lowering the quality of life for riverfront residents at the type locality. RESULTS We tested the efficacy and potential mobility of a transfluthrin-based paint (a.i. 0.50%), comparing the impacts of UV exposure and substrate texture over time. Direct UV exposure decreased efficacy (β ± S.E. = 0.008 ± 0.001, P < 0.001) and a coarse texture maintained greater efficacy (β ± S.E. = −3.7 ± 1.3, P = 0.004) over time. Notably, the coarse texture + indirect UV treatment maintained 100% mortality after 240 days. UV exposure and substrate texture did not have a significant impact on leachate concentrations over time, and successive immersion tests indicated a two-phase emission pattern. Bioaccumulation increased with time on the cuticle of dead adult S. fasciatella ; after 24 h of direct exposure the concentration of transfluthrin was 25.3 ± 0.9 ng/caddisfly with a maximum concentration of 345 ng/caddisfly after 7 days. CONCLUSION Our predictions were validated with measured, time-dependent impacts on efficacy, leachability, and bioaccumulation. Because of the mobility of active ingredient in the environment, insecticidal paints merit low-impact protocols to improve public health outcomes and environmental safety. © 2022 Society of Chemical Industry.

Pest Management Science

Linking metal bioaccumulation of aquatic insects to their distribution patterns in a mining-impacted river

Although the differential responses of stream taxa to metal exposure have been exploited for bioassessment and monitoring, the mechanisms affecting these responses are not well understood. In this study, the subcellular partitioning of metals in operationally defined metal-sensitive and detoxified fractions were analyzed in five insect taxa. Samples were collected in two separate years along an extensive metal contamination gradient in the Clark Fork River (MT, USA) to determine if interspecific differences in the metal concentrations of metal-sensitive fractions and detoxified fractions were linked to the differences in distributions of taxa relative to the gradient. Most of the Cd, Cu, and Zn body burdens were internalized and potentially biologically active in all taxa, although all taxa appeared to detoxify metals (e.g., metal bound to cytosolic metal-binding proteins). Metal concentrations associated with metal-sensitive fractions were highest in the mayflies Epeorus albertae and Serratella tibialis , which were rare or absent from the most contaminated sites but occurred at less contaminated sites. Relatively low concentrations of Cu were common to the tolerant taxa Hydropsyche spp. and Baetis spp., which were widely distributed and dominant in the most contaminated sections of the river. This suggested that distributions of taxa along the contamination gradient were more closely related to the bioaccumulation of Cu than of other metals. Metal bioaccumulation did not appear to explain the spatial distribution of the caddisfly Arctopsyche grandis , considered to be a bioindicator of metal effects in the river. Thus, in this system the presence/absence of most of these taxa from sites where metal exposure was elevated could be differentiated on the basis of differences in metal bioaccumulation.

Montana

Growth and secondary production of aquatic insects along a gradient of Zn contamination in Rocky Mountain streams

Secondary production estimates from several Rocky Mountain streams were used to test hypotheses about the effects of chronic metal contamination on insect populations and ecosystem processes. Quantitative samples of chemistry, habitat, and benthic insects were collected monthly during the ice-free period (May–November) from five 2 nd - to 3 rd -order streams that varied primarily in Zn contamination. Secondary production was estimated for the 19 dominant taxa using increment-summation, size-frequency, and P/B methods. Uncertainty was estimated by bootstrapping estimates of mean abundance, biomass, and cohort production intervals. Secondary production of metal-sensitive Heptageniidae ( Rhithrogena robusta , Cinygmula spp., and Epeorus longimanus ) was lower in lightly to moderately contaminated streams than in reference streams. Experiments were done to determine whether herbivore growth was influenced by food quality in contaminated streams. Growth estimates from field and microcosm experiments revealed that low mayfly production in contaminated streams was caused mostly by reduced population abundances. Production of predatory stoneflies was also lower in contaminated streams than reference streams. Estimates of the trophic basis of production revealed that, although the relative contribution to community production from various food sources was similar among streams, total production attributable to algae and animal prey declined in contaminated streams. Much of the reduction in herbivory in contaminated streams was the result of lower production of heptageniids, especially R. robusta . Assemblage and taxon-specific estimates of secondary production were sensitive to variation in metal contamination and indicated that relatively low metal concentrations may have ecosystem-wide consequences for energy flow.

Journal of the North American Benthological Societ

Invertebrate prey contributions to juvenile Coho Salmon diet from riparian habitats along three Alaska streams: Implications for environmental change

Stream fish rely on a mix of terrestrial and aquatic prey sources. While the importance of terrestrial invertebrates as a food source for stream fish is well documented, the role of aquatic insects that emerge from the stream as winged adult insects (aquatic winged adults) and return to the stream as prey is less understood. In this study we determined the proportion of total diet for stream-rearing juvenile Coho Salmon ( Oncorhynchus kisutch) that is derived from terrestrial and aquatic winged adult invertebrates which enter the stream from riparian habitats and consider how those cross-ecosystem prey contributions vary based on riparian habitat type. Study reaches were identified in three streams within the Kenai River watershed of Alaska that were representative of habitats found throughout the region and riparian vegetation was classified into grass/sedge, shrub and tree types using LiDAR. Juvenile Coho Salmon stomach contents were sampled seasonally in study reaches over a two-year period and ingested invertebrates were identified by taxa, life stage and origin. Our results showed that aquatic winged adult prey contributions to juvenile salmon diet were significantly lower in the grass/sedge study reach, and cross-ecosystem invertebrate prey represented a significantly higher proportion of juvenile salmon diet in the tree study reach. Invertebrate prey in the grass/sedge reach were composed primarily of the larval life stage of aquatic winged adults. These results suggest that change in riparian vegetation from tree/shrub to grass/sedge along Kenai streams as projected by regional climate change models, or that results from anthropogenic modification, will likely lead to lower availability of cross-ecosystem prey for stream fish. Management of riparian buffers along streams to preserve or increase occurrence of trees and shrubs is likely to help mitigate impacts of those possible changes.

Alaska

An ecosystem-scale model of PFAS dynamics in stream-to-riparian food webs

Per- and polyfluoroalkyl substances (PFAS) are widespread contaminants in aquatic ecosystems, where they bioaccumulate and trophically transfer through food webs. We derived an ecosystem-scale model assessing Σ 12 PFAS partitioning, bioaccumulation by larval aquatic insects, bioamplification by adult aquatic insects, and trophic transfer from aquatic insects to riparian spiders using data collected across five streams in a mildly impacted watershed. Partitioning involved the greatest PFAS enrichments (range in posterior median log 10 k d values = 1.5–2.1), with lesser concentration increases from particulates to larval aquatic insects and from larval to adult aquatic insects, and Σ 12 PFAS concentration decreases from adult aquatic insects to spiders. Among the 12 compounds, PFOS had the largest proportional contribution to Σ 12 PFAS concentrations for all sample types, with consistently increasing concentrations from surface water to adult aquatic insects. Σ 12 PFAS concentrations (5.4–51 ppb wet weight), body burdens (0.44–5.2 ng per individual), and bioamplification factors (0.15–4.9) differed considerably among five common aquatic insect taxa. This study presents a robust modeling framework for PFAS trophodynamics and offers insights into the biological controls that contribute to the context dependency of PFAS at the interfaces of aquatic and terrestrial food webs.

Connecticut, Massachusetts

Cross-ecosystem linkages and trace metals at the land-water interface

At low concentrations, trace metals are critical for sustaining life on Earth. However, at high concentrations, they become a global contaminant with particularly strong effects on freshwater communities. These effects can propagate to terrestrial ecosystems in part by altering production and community structure of adult aquatic insect emergence and aquatic insect-mediated metal fluxes to terrestrial insectivores. Here we highlight mechanisms driving effects of trace metals on aquatic organisms in general, aquatic insects specifically, and insectivorous consumers at the land-water interface. Specifically, we focus on how trace metals impact and bioaccumulate in aquatic organisms and communities and how these changes propagate through aquatic food web interactions and insect metamorphosis to alter fluxes of aquatically derived prey and trace metals to terrestrial consumers. Ultimately, trace metals impact food webs at the land-water interface by altering aquatic insect prey composition and availability for aquatic insectivores and by reducing aquatic insect subsidies to terrestrial consumers, and not by increasing exposure to trace metals in prey. Exposure of terrestrial insectivores to trace metals in prey is decoupled from aqueous concentrations due to high rates of metal excretion during insect metamorphosis from aquatic larvae to terrestrial adult. These effects increase reliance of aquatic insectivores on terrestrial insect prey subsidies and/or lead to declines and behavioral changes in terrestrial insectivore populations.

Book chapter

Effects of chronic metal exposure and metamorphosis on the microbiomes of larval and adult insects and riparian spiders through the aquatic-riparian food web

The macroinvertebrate microbiome controls various aspects of the host's physiology, from regulation of environmental contaminants to reproductive output. Aquatic insects provide critical nutritional subsidies linking aquatic and riparian food webs while simultaneously serving as a contaminant pathway for riparian insectivores in polluted ecosystems. Previous studies have characterized the transport and transfer of contaminants from aquatic to riparian ecosystems through insect metamorphosis, but both contaminant exposure and metamorphosis are energetically intensive processes that may cause host microbiomes to undergo radical transformation in structure and function, potentially affecting the host's physiology. We collected arthropods from three sites within Torch Lake, a historical copper mine in the Keweenaw Peninsula, Michigan, USA, and three sites within a nearby reference lake. Our objectives were to: 1) characterize the variation in microbiome communities and predicted metagenomic functions with legacy copper mining activity across space, among host types and family-level host taxonomy, 2) characterize how insect metamorphosis alters the microbiome community, including the degree of endosymbiotic infection, and predicted metagenomic function. We field-collected organisms, extracted their DNA, and sequenced the 16S region of the rRNA gene to characterize microbiome communities, then predicted metagenomic function. Site, lake, and host taxonomy affected the host microbiome community composition. Copper exposure increased the abundance of xenobiotic and lipid metabolism pathways in the Araneidae spider microbiome. Insect metamorphosis reduced the alpha diversity, altered the community composition, and predicted metagenomic function. We observed a bioconcentration of endosymbiotic bacteria in adult insects, especially holometabolous insects. Through metamorphosis, we observed a transition in function from xenobiotic degradation pathways to carbohydrate metabolism. Overall, contaminant exposure alters the microbiome composition in aquatic insects and riparian spiders and alters the function of the microbiome across the aquatic-riparian interface. Furthermore, metamorphosis is a critical element in shaping the aquatic insect microbiome across its life history.

Michigan

Baseline assessment of fish communities, benthic macroinvertebrate communities, and stream habitat and land use, Big Thicket National Preserve, Texas, 1999-2001

The Big Thicket National Preserve comprises 39,300 hectares in the form of nine preserve units connected by four stream corridor units (with two more corridor units proposed) distributed over the lower Neches and Trinity River Basins of southeastern Texas. Fish and benthic macroinvertebrate data were collected at 15 stream sites (reaches) in the preserve during 1999–2001 for a baseline assessment and a comparison of communities among stream reaches. The fish communities in the preserve were dominated by minnows (family Cyprinidae) and sunfishes (family Centrarchidae). Reaches with smaller channel sizes generally had higher fish species richness than the larger reaches in the Neches River and Pine Island Bayou units of the preserve. Fish communities in geographically adjacent reaches were most similar in overall community structure. The blue sucker, listed by the State as a threatened species, was collected in only one reach—a Neches River reach a few miles downstream from the Steinhagen Lake Dam. Riffle beetles (family Elmidae) and midges (family Chironomidae) dominated the aquatic insect communities at the 14 reaches sampled for aquatic insects in the preserve. The Ephemeroptera, Plecoptera and Trichoptera (EPT) Index, an index sensitive to water-quality degradation, was smallest at the Little Pine Island Bayou near Beaumont reach that is in a State 303(d)-listed stream segment on Little Pine Island Bayou. Trophic structure of the aquatic insect communities is consistent with the river continuum concept with shredder and scraper insect taxa more abundant in reaches with smaller stream channels and filter feeders more abundant in reaches with larger channels. Aquatic insect community metrics were not significantly correlated to any of the stream-habitat or land-use explanatory variables. The percentage of 1990s urban land use in the drainage areas upstream from 12 bioassessment reaches were negatively correlated to the reach structure index, which indicates less stable habitat for aquatic biota.

Texas