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      Heavy metal movement through insect food chains in pristine thermal springs of Yellowstone National Park


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          Yellowstone National Park thermal features regularly discharge various heavy metals and metalloids. These metals are taken up by microorganisms that often form mats in thermal springs. These microbial mats also serve as food sources for invertebrate assemblages. To examine how heavy metals move through insect food webs associated with hot springs, two sites were selected for this study. Dragon-Beowulf Hot Springs, acid-sulfate chloride springs, have a pH of 2.9, water temperatures above 70 °C, and populations of thermophilic bacterial, archaeal, and algal mats. Rabbit Creek Hot Springs, alkaline springs, have a pH of up to 9, some water temperatures in excess of 60 °C, and are populated with thermophilic and phototrophic bacterial mats. Mats in both hydrothermal systems form the trophic base and support active metal transfer to terrestrial food chains. In both types of springs, invertebrates bioaccumulated heavy metals including chromium, manganese, cobalt, nickel, copper, cadmium, mercury, tin and lead, and the metalloids arsenic, selenium, and antimony resulting from consuming the algal and bacterial mat biomass. At least two orders of magnitude increase in concentrations were observed in the ephydrid shore fly Paracoenia turbida, as compared to the mats for all metals except antimony, mercury, and lead. The highest bioaccumulation factor (BAF) of 729 was observed for chromium. At the other end of the food web, the invertebrate apex predator, Cicindelidia haemorrhagica, had at least a 10-fold BAF for all metals at some location-year combinations, except with antimony. Of other taxa, high BAFs were observed with zinc for Nebria sp. (2180) and for Salda littoralis (1080). This accumulation, occurring between primary producer and primary consumer trophic levels at both springs, is biomagnified through the trophic web. These observations suggest trace metals enter the geothermal food web through the microbial mat community and are then transferred through the food chain. Also, while bioaccumulation of arsenic is uncommon, we observed five instances of increases near or exceeding 10-fold: Odontomyia sp. larvae (13.6), P. turbida (34.8), C. haemorrhagica (9.7), Rhagovelia distincta (16.3), and Ambrysus mormon (42.8).

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          Heavy metal toxicity and the environment.

          Heavy metals are naturally occurring elements that have a high atomic weight and a density at least five times greater than that of water. Their multiple industrial, domestic, agricultural, medical, and technological applications have led to their wide distribution in the environment, raising concerns over their potential effects on human health and the environment. Their toxicity depends on several factors including the dose, route of exposure, and chemical species, as well as the age, gender, genetics, and nutritional status of exposed individuals. Because of their high degree of toxicity, arsenic, cadmium, chromium, lead, and mercury rank among the priority metals that are of public health significance. These metallic elements are considered systemic toxicants that are known to induce multiple organ damage, even at lower levels of exposure. They are also classified as human carcinogens (known or probable) according to the US Environmental Protection Agency and the International Agency for Research on Cancer. This review provides an analysis of their environmental occurrence, production and use, potential for human exposure, and molecular mechanisms of toxicity, genotoxicity, and carcinogenicity.
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            Bar-coded pyrosequencing reveals shared bacterial community properties along the temperature gradients of two alkaline hot springs in Yellowstone National Park.

            An understanding of how communities are organized is a fundamental goal of ecology but one which has historically been elusive for microbial systems. We used a bar-coded pyrosequencing approach targeting the V3 region of the bacterial small-subunit rRNA gene to address the factors that structure communities along the thermal gradients of two alkaline hot springs in the Lower Geyser Basin of Yellowstone National Park. The filtered data set included a total of nearly 34,000 sequences from 39 environmental samples. Each was assigned to one of 391 operational taxonomic units (OTUs) identified by their unique V3 sequence signatures. Although the two hot springs differed in their OTU compositions, community resemblance and diversity changed with strikingly similar dynamics along the two outflow channels. Two lines of evidence suggest that these community properties are controlled primarily by environmental temperature. First, community resemblance decayed exponentially with increasing differences in temperature between samples but was only weakly correlated with physical distance. Second, diversity decreased with increasing temperature at the same rate along both gradients but was uncorrelated with other measured environmental variables. This study also provides novel insights into the nature of the ecological interactions among important taxa in these communities. A strong negative association was observed between cyanobacteria and the Chloroflexi, which together accounted for approximately 70% of the sequences sampled. This pattern contradicts the longstanding hypothesis that coadapted lineages of these bacteria maintain tightly cooccurring distributions along these gradients as a result of a producer-consumer relationship. We propose that they instead compete for some limiting resource(s).
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              Factors controlling the bioaccumulation of mercury, methylmercury, arsenic, selenium, and cadmium by freshwater invertebrates and fish.

              Concentrations of mercury (Hg), methylmercury (MMHg), arsenic (As), selenium (Se), and cadmium (Cd) were measured in atmospheric deposition, stream water, and biota in two streams in western Maryland. Overall, concentrations were slightly higher in the water of the lower pH Herrington Creek tributary (HRCT). Bioaccumulation factors were also higher for HRCT compared to Blacklick Run (BLK). MMHg concentrations in biota increased with trophic level and essentially all the Hg was as MMHg in predatory insects and insectivorous/carnivorous fish. Thus, the overall trophic status of the organism was indicated by the %MMHg in its tissues. Levels of As, Se, Cd, and Hg, however, decreased with increasing trophic level. Adsorption of As to the exoskeleton of invertebrates appears to be an important accumulation mechanism. MMHg was distributed evenly throughout crayfish and fish organs, whereas As, Se, Cd, and Hg were found in higher concentrations in detoxifying organs. Concentrations in biota in this study were somewhat elevated compared to other rural sites, but were less than those of point source-contaminated sites. Overall, as atmospheric inputs to the two watersheds were similar, the results of this study show the importance of water chemistry in determining the bioaccumulation of the metals and metalloids into insects. Subsequent transfer to higher trophic levels is related to both the ability of the organisms to depurate and the mode of accumulation, either directly from water or from food.

                Author and article information

                PeerJ Inc. (San Diego, USA )
                21 February 2024
                : 12
                : e16827
                [1 ]Department of Plant Pathology, Entomology, and Microbiology, Iowa State University , Ames, IA, United States of America
                [2 ]Department of Land Resources & Environmental Sciences, Montana State University , Bozeman, MT, United States of America
                [3 ]School of Natural Resources, University of Nebraska-Lincoln , Lincoln, NE, United States of America
                [4 ]Yellowstone National Park , Gardner, MT, United States of America
                ©2024 Adams et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

                : 20 November 2023
                : 3 January 2024
                Funded by: Therion, LLC, Brian Fiske, the Robert Allen Wright Endowment of Iowa State University, Montana State University, and the Montana Agricultural Experiment Station, and the University of Nebraska-Lincoln
                This study was supported with assistance from Therion, LLC, Brian Fiske, the Robert Allen Wright Endowment of Iowa State University, Montana State University, and the Montana Agricultural Experiment Station, and the University of Nebraska-Lincoln. There was no additional external funding received for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.



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