Bioaccumulation of contaminants in Scarabaeidae and Silphidae beetles at sites polluted by coal combustion residuals and radiocesium

Silva, Ansley E.; Speakman, Robert J.; Barnes, Brittany F.; Coyle, David R.; Leaphart, James C.; Abernethy, Erin F.; Turner, Kelsey L.; Rhodes, Jr., Olin E.; Beasley, James C.; Gandhi, Kamal J. K.

doi:10.1016/j.scitotenv.2023.166821

Title: Bioaccumulation of contaminants in Scarabaeidae and Silphidae beetles at sites polluted by coal combustion residuals and radiocesium

Journal Article · 09 September 2023 · Science of the Total Environment

DOI: https://doi.org/10.1016/j.scitotenv.2023.166821 · OSTI ID:2203425

Silva, Ansley E. ^[1]; Speakman, Robert J. ^[1]; Barnes, Brittany F. ^[1]; Coyle, David R. ^[2]; Leaphart, James C. ^[3]; Abernethy, Erin F. ^[4]; Turner, Kelsey L. ^[3]; Rhodes, Jr., Olin E. ^[4]; Beasley, James C. ^[3]; Gandhi, Kamal J. K. ^[1]

University of Georgia, Athens, GA (United States)
University of Georgia, Athens, GA (United States); Clemson University, SC (United States)
University of Georgia, Athens, GA (United States); University of Georgia, Aiken, SC (United States); Savannah River Ecology Laboratory (SREL), Aiken, SC (United States)
University of Georgia, Aiken, SC (United States); Savannah River Ecology Laboratory (SREL), Aiken, SC (United States); University of Georgia, Athens, GA (United States)

Anthropogenic contamination from coal-fired power plants and nuclear reactors is a pervasive issue impacting ecosystems across the globe. As a result, it is critical that studies continue to assess the accumulation and effects of trace elements and radionuclides in a diversity of biota. In particular, bioindicator species are a powerful tool for risk assessment of chemically contaminated habitats. Using inductively coupled plasma mass spectrometry (ICP-MS) and auto-gamma counting, we analyzed trace element and radiocesium contaminant concentrations in Scarabaeidae and Silphidae beetles (Order: Coleoptera), important taxa in decomposition and nutrient cycling, at contaminated and reference sites on the Savannah River Site, South Carolina, U.S. Our results revealed variability in trace element concentrations between Scarabaeidae and Silphidae beetles at uncontaminated and contaminated sites. Compared to Scarabaeidae, Silphidae had higher levels of chromium (Cr), copper (Cu), iron (Fe), manganese (Mn), nickel (Ni), and zinc (Zn). Unexpectedly, concentrations of Cr, Cu, and Ni were higher in both taxa at the uncontaminated sites. Scarabaeidae and Silphidae beetles at the coal combustion waste site consistently had high concentrations of arsenic (As), and Scarabaeidae had high concentrations of selenium (Se). Of the 50 beetles analyzed for radiocesium levels, two had elevated radioactivity concentrations, both of which were from a site contaminated with radionuclides. Furthermore, our results suggest carrion beetles may be particularly sensitive to bioaccumulation of contaminants due to their trophic position and role in decomposition, and thus are useful sentinels of trace element and radionuclide contamination.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Savannah River Ecology Laboratory (SREL), Aiken, SC (United States)

Sponsoring Organization:: USDOE Office of Environmental Management (EM)

Grant/Contract Number:: EM0005228

OSTI ID:: 2203425

Journal Information:: Science of the Total Environment, Vol. 904; ISSN 0048-9697

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (60)

Inventory and spatial pattern of in a pond: a comparison of two survey methods Abraham, J. P.; Whicker, F. W.; Hinton, T. G. Journal of Environmental Radioactivity, Vol. 51, Issue 2 https://doi.org/10.1016/S0265-931X(00)00052-7	journal	November 2000
Hepatic and renal trace element concentrations in American alligators (Alligator mississippiensis) following chronic dietary exposure to coal fly ash contaminated prey Tuberville, Tracey D.; Scott, David E.; Metts, Brian S. Environmental Pollution, Vol. 214 https://doi.org/10.1016/j.envpol.2016.04.003	journal	July 2016
Recovery of novel bacterial diversity from a forested wetland impacted by reject coal: Community changes along a coal contamination gradient Brofft, Jennifer E.; McArthur, J. Vaun; Shimkets, Lawrence J. Environmental Microbiology, Vol. 4, Issue 11 https://doi.org/10.1046/j.1462-2920.2002.00337.x	journal	November 2002
Thallium Contamination of Water in Canada Cheam, Ven Water Quality Research Journal, Vol. 36, Issue 4 https://doi.org/10.2166/wqrj.2001.046	journal	November 2001
Addressing ecological effects of radiation on populations and ecosystems to improve protection of the environment against radiation: Agreed statements from a Consensus Symposium Bréchignac, François; Oughton, Deborah; Mays, Claire Journal of Environmental Radioactivity, Vol. 158-159 https://doi.org/10.1016/j.jenvrad.2016.03.021	journal	July 2016
Heavy metal concentrations in ground beetles, leaf litter, and soil of a forest ecosystem Jelaska, Lucija Šerić; Blanuša, Maja; Durbešić, Paula Ecotoxicology and Environmental Safety, Vol. 66, Issue 1 https://doi.org/10.1016/j.ecoenv.2005.10.017	journal	January 2007
Heavy metal bioaccumulation in two passerines with differing migration strategies Cooper, Zoë; Bringolf, Robert; Cooper, Robert Science of The Total Environment, Vol. 592 https://doi.org/10.1016/j.scitotenv.2017.03.055	journal	August 2017
A life-cycle theory of responses to stress Sibly, R. M.; Calow, P. Biological Journal of the Linnean Society, Vol. 37, Issue 1-2 https://doi.org/10.1111/j.1095-8312.1989.tb02007.x	journal	May 1989
Selenium in Fly Ash Gutenmann, Walter H.; Bache, Carl A.; Youngs, William D. Science, Vol. 191, Issue 4230 https://doi.org/10.1126/science.1251212	journal	March 1976
Trophic status and metal bioaccumulation differences in multiple fish species exposed to coal ash-associated metals Otter, Ryan R.; Bailey, Frank C.; Fortner, Allison M. Ecotoxicology and Environmental Safety, Vol. 85 https://doi.org/10.1016/j.ecoenv.2012.08.022	journal	November 2012
The influence of soil characteristics on the toxicity of four chemicals to the earthworm Eisenia fetida andrei (Oligochaeta) van Gestel, C. A. M.; van Dis, W. A. Biology and Fertility of Soils, Vol. 6, Issue 3 https://doi.org/10.1007/BF00260822	journal	May 1988
Radiocesium contamination of the web spider Nephila clavata (Nephilidae: Arachnida) 1.5 years after the Fukushima Dai-ichi Nuclear Power Plant accident Ayabe, Yoshiko; Kanasashi, Tsutomu; Hijii, Naoki Journal of Environmental Radioactivity, Vol. 127 https://doi.org/10.1016/j.jenvrad.2013.10.010	journal	January 2014
GPS-coupled contaminant monitors on free-ranging Chernobyl wolves challenge a fundamental assumption in exposure assessments Hinton, Thomas G.; Byrne, Michael E.; Webster, Sarah C. Environment International, Vol. 133 https://doi.org/10.1016/j.envint.2019.105152	journal	December 2019
ES&T Special Report: Priority pollutants: I-a perspective view Keith, Larry; Telliard, William Environmental Science & Technology, Vol. 13, Issue 4 https://doi.org/10.1021/es60152a601	journal	April 1979
Lead and Cadmium in Soil and Isopoda Woodlice in Croatia Blanuša, Maja; Mrković-Milić, Romana; Durbešić, Paula Ecotoxicology and Environmental Safety, Vol. 52, Issue 3 https://doi.org/10.1006/eesa.2002.2173	journal	July 2002
Plutonium, 137Cs and 90Sr in selected invertebrates from some areas around Chernobyl nuclear power plant Mietelski, Jerzy W.; Maksimova, Svetlana; Szwałko, Przemysław Journal of Environmental Radioactivity, Vol. 101, Issue 6 https://doi.org/10.1016/j.jenvrad.2008.04.009	journal	June 2010
Use of Single Extraction Methods to Predict Bioavailability of Heavy Metals in Polluted Soils to Rice Zhang, Ming-Kui; Liu, Zhao-Yun; Wang, Huo Communications in Soil Science and Plant Analysis, Vol. 41, Issue 7 https://doi.org/10.1080/00103621003592341	journal	March 2010
Linking Metal Bioaccumulation of Aquatic Insects to Their Distribution Patterns in a Mining-Impacted River Cain, Daniel J.; Luoma, Samuel N.; Wallace, William G. Environmental Toxicology and Chemistry, Vol. 23, Issue 6 https://doi.org/10.1897/03-291	journal	January 2004
Effects of Ionizing Radiation on Terrestrial Ecosystems: Experiments show how ionizing radiation may alter normally stable patterns of ecosystem behavior Woodwell, G. M. Science, Vol. 138, Issue 3540 https://doi.org/10.1126/science.138.3540.572	journal	November 1962
Wildlife and the Coal Waste Policy Debate: Proposed Rules for Coal Waste Disposal Ignore Lessons from 45 Years of Wildlife Poisoning Lemly, A. Dennis; Skorupa, Joseph P. Environmental Science & Technology, Vol. 46, Issue 16 https://doi.org/10.1021/es301467q	journal	August 2012
Metal Kinetics and Respiration Rates in F1 Generation of Carabid Beetles (Pterostichus oblongopunctatus F.) Originating From Metal-Contaminated and Reference Areas Lagisz, M.; Kramarz, P.; Niklinska, M. Archives of Environmental Contamination and Toxicology, Vol. 48, Issue 4 https://doi.org/10.1007/s00244-004-0023-2	journal	March 2005
Contaminant bioavailability in soils, sediments, and aquatic environments Traina, S. J.; Laperche, V. Proceedings of the National Academy of Sciences, Vol. 96, Issue 7 https://doi.org/10.1073/pnas.96.7.3365	journal	March 1999
Effects of competition and coal-combustion wastes on recruitment and life history characteristics of salamanders in temporary wetlands Roe, John H.; Hopkins, William A.; DuRant, Sarah E. Aquatic Toxicology, Vol. 79, Issue 2 https://doi.org/10.1016/j.aquatox.2006.06.007	journal	August 2006
The Social Behavior of Burying Beetles Milne, Lorus J.; Milne, Margery Scientific American, Vol. 235, Issue 2 https://doi.org/10.1038/scientificamerican0876-84	journal	August 1976
Methods for Speciation of Metals in Soils D'Amore, J. J.; Al‐Abed, S. R.; Scheckel, K. G. Journal of Environmental Quality, Vol. 34, Issue 5 https://doi.org/10.2134/jeq2004.0014	journal	September 2005
Toxic Metals in Surface Waters from coal ash Cherry, D. S.; Guthrie, R. K. Journal of the American Water Resources Association, Vol. 13, Issue 6 https://doi.org/10.1111/j.1752-1688.1977.tb02093.x	journal	December 1977
Using Raccoons as an Indicator Species for Metal Accumulation across Trophic Levels: A Stable Isotope Approach Gaines, Karen F.; Romanek, Christopher S.; Boring, C. Shane The Journal of Wildlife Management, Vol. 66, Issue 3 https://doi.org/10.2307/3803145	journal	July 2002
Effect of clay and organic matter type on the ecotoxicity of zinc and cadmium to the potworm Enchytraeus albidus Lock, Koen; Janssen, Colin R. Chemosphere, Vol. 44, Issue 8 https://doi.org/10.1016/S0045-6535(00)00565-8	journal	September 2001
Effects of industrial disturbances on biodiversity of carrion-associated beetles Silva, Ansley E.; Barnes, Brittany F.; Coyle, David R. Science of The Total Environment, Vol. 709 https://doi.org/10.1016/j.scitotenv.2019.135158	journal	March 2020
Dispersal of heavy metals from abandoned mine workings and their transference through terrestrial food chains Roberts, R. D.; Johnson, M. S. Environmental Pollution (1970), Vol. 16, Issue 4 https://doi.org/10.1016/0013-9327(78)90080-0	journal	August 1978
Costs of living in metal polluted areas: respiration rate of the ground beetle Pterostichus oblongopunctatus from two gradients of metal pollution Bednarska, Agnieszka J.; Stachowicz, Izabela Ecotoxicology, Vol. 22, Issue 1 https://doi.org/10.1007/s10646-012-1008-y	journal	October 2012
Patterns of Trace Element Accumulation in Waterfowl Restricted to Impoundments Holding Coal Combustion Waste Leaphart, James C.; Oldenkamp, Ricki E.; Bryan, Albert L. Environmental Toxicology and Chemistry, Vol. 39, Issue 5 https://doi.org/10.1002/etc.4697	journal	April 2020
Survey of the Potential Environmental and Health Impacts in the Immediate Aftermath of the Coal Ash Spill in Kingston, Tennessee Ruhl, Laura; Vengosh, Avner; Dwyer, Gary S. Environmental Science & Technology, Vol. 43, Issue 16 https://doi.org/10.1021/es900714p	journal	August 2009
Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China Khan, S.; Cao, Q.; Zheng, Y. M. Environmental Pollution, Vol. 152, Issue 3 https://doi.org/10.1016/j.envpol.2007.06.056	journal	April 2008
Metal accumulation in soil arthropods in relation to micro-nutrients Janssen, Martien P. M.; Hogervorst, RenéF. Environmental Pollution, Vol. 79, Issue 2 https://doi.org/10.1016/0269-7491(93)90068-Y	journal	January 1993
Distribution of Long-Lived Radionuclides in an Abandoned Reactor Cooling Reservoir Whicker, F. Ward; Pinder, John E.; Bowling, John W. Ecological Monographs, Vol. 60, Issue 4 https://doi.org/10.2307/1943017	journal	February 1990
Toxicity and bioaccumulation of thallium in Hyalella azteca, with comparison to other metals and prediction of environmental impact Borgmann, U.; Cheam, V.; Norwood, W. P. Environmental Pollution, Vol. 99, Issue 1 https://doi.org/10.1016/S0269-7491(97)00181-4	journal	January 1998
Trace elements and radiocesium in game species near contaminated sites: Game Species Contamination Risk Oldenkamp, Ricki E.; Bryan, Albert L.; Kennamer, Robert A. The Journal of Wildlife Management, Vol. 81, Issue 8 https://doi.org/10.1002/jwmg.21314	journal	August 2017
Why Is Metal Bioaccumulation So Variable? Biodynamics as a Unifying Concept Luoma, Samuel N.; Rainbow, Philip S. Environmental Science & Technology, Vol. 39, Issue 7 https://doi.org/10.1021/es048947e	journal	April 2005
Geotrupine beetles (Coleoptera: Scarabaeoidea) as bio-monitors of man-made radioactivity Mietelski, Jerzy W.; Szwałko, Przemysław; Tomankiewicz, Ewa Journal of Environmental Monitoring, Vol. 5, Issue 2 https://doi.org/10.1039/b212592g	journal	February 2003
Selenium, arsenic, and mercury in fish inhabiting a fly ash exposure gradient: interspecific bioaccumulation patterns and elemental associations Reash, Robin J. Environmental Toxicology and Chemistry, Vol. 31, Issue 4 https://doi.org/10.1002/etc.1745	journal	February 2012
The Ecology of Serpentine Soils Whittaker, R. H. Ecology, Vol. 35, Issue 2 https://doi.org/10.2307/1931126	journal	April 1954
Maternal Transfer of Contaminants and Reduced Reproductive Success of Southern Toads (Bufo [Anaxyrus] terrestris) Exposed to Coal Combustion Waste Metts, Brian S.; Buhlmann, Kurt A.; Tuberville, Tracey D. Environmental Science & Technology, Vol. 47, Issue 6 https://doi.org/10.1021/es303989u	journal	February 2013
Radionuclide behaviour and transport in a coniferous woodland ecosystem: vegetation, invertebrates and wood mice, Apodemus sylvaticus Copplestone, D.; Johnson, M. S.; Jones, S. R. Science of The Total Environment, Vol. 239, Issue 1-3 https://doi.org/10.1016/S0048-9697(99)00294-6	journal	October 1999
Reduced survival and body size in the terrestrial isopod Porcellio scaber from a metal-polluted environment Jones, D. T.; Hopkin, S. P. Environmental Pollution, Vol. 99, Issue 2 https://doi.org/10.1016/S0269-7491(97)00188-7	journal	January 1998
Subsurface leachate migration from a reject coal pile in South Carolina Carlsonn, CatherineA. Water, Air, and Soil Pollution, Vol. 53, Issue 3-4 https://doi.org/10.1007/BF00170748	journal	October 1990
Integration of ecosystem science into radioecology: A consensus perspective Rhodes, Olin E.; Bréchignac, Francois; Bradshaw, Clare Science of The Total Environment, Vol. 740 https://doi.org/10.1016/j.scitotenv.2020.140031	journal	October 2020
Terrestrial and Aquatic Invertebrates as Bioindicators for Environmental Monitoring, with Particular Reference to Mountain Ecosystems Hodkinson, Ian D.; Jackson, John K. Environmental Management, Vol. 35, Issue 5 https://doi.org/10.1007/s00267-004-0211-x	journal	May 2005
Influence of relative trophic position and carbon source on selenium bioaccumulation in turtles from a coal fly-ash spill site Van Dyke, James U.; Hopkins, William A.; Jackson, Brian P. Environmental Pollution, Vol. 182 https://doi.org/10.1016/j.envpol.2013.06.025	journal	November 2013
Metal accumulation in arthropods near a lead/zinc smelter in Arnoldstein, Austria. I Rabitsch, Wolfgang B. Environmental Pollution, Vol. 90, Issue 2 https://doi.org/10.1016/0269-7491(94)00082-O	journal	January 1995
Mercury levels and its chemical form in tissues and organs of seabirds Kim, E. Y.; Murakami, T.; Saeki, K. Archives of Environmental Contamination and Toxicology, Vol. 30, Issue 2 https://doi.org/10.1007/BF00215806	journal	February 1996
Time to death response in carabid beetles exposed to multiple stressors along a gradient of heavy metal pollution Stone, D.; Jepson, P.; Kramarz, P. Environmental Pollution, Vol. 113, Issue 2 https://doi.org/10.1016/S0269-7491(00)00134-2	journal	July 2001
The Internal Distribution of Nickel and Thallium in Two Freshwater Invertebrates and its Relevance to Trophic Transfer Dumas, Julie; Hare, Landis Environmental Science & Technology, Vol. 42, Issue 14 https://doi.org/10.1021/es800378j	journal	June 2008
Passage of metals in effluents, through bacteria to higher organisms Patrick, F.; Loutit, M. Water Research, Vol. 10, Issue 4 https://doi.org/10.1016/0043-1354(76)90176-7	journal	January 1976
Metal concentrations in soil and invertebrates in the vicinity of a metallurgical factory near Tula (Russia) van Straalen, Nico M.; Butovsky, Ruslan O.; Pokarzhevskii, Andrei D. Pedobiologia, Vol. 45, Issue 5 https://doi.org/10.1078/0031-4056-00099	journal	January 2001
Ecotoxicoparasitology of mercury and trace elements in semi-aquatic mammals and their endoparasite communities Borchert, Ernest J.; Leaphart, James C.; Bryan, Albert L. Science of The Total Environment, Vol. 679 https://doi.org/10.1016/j.scitotenv.2019.04.326	journal	August 2019
Environmental fate of radiocesium in biota inhabiting a contaminated ecosystem on the U.S. Department of Energy's Savannah River Site Leaphart, James C.; Korotasz, Alexis M.; Bryan, Albert L. Journal of Environmental Radioactivity, Vol. 222 https://doi.org/10.1016/j.jenvrad.2020.106321	journal	October 2020
Radiation-Induced Effects on Plants and Animals: Findings of the United Nations Chernobyl Forum Hinton, Thomas G.; Alexakhin, Rudolph; Balonov, Mikhail Health Physics, Vol. 93, Issue 5 https://doi.org/10.1097/01.HP.0000281179.03443.2e	journal	January 2007
Copper and zinc contents in trophic chains of terrestrial arthropods in the Moscow region Butovsky, R. O.; Van Straalen, N. M. Pedobiologia, Vol. 39, Issue 6 https://doi.org/10.1016/S0031-4056(24)00215-4	journal	November 1995
Investigations on lead in the soil invertebrates of a forest ecosystem Roth, Mechthild Pedobiologia, Vol. 37, Issue 5 https://doi.org/10.1016/S0031-4056(24)00103-3	journal	September 1993

Similar Records

Effects of industrial disturbances on biodiversity of carrion-associated beetles

Journal Article · 2019 · Science of the Total Environment · OSTI ID:1814833

Silva, Ansley E.; Barnes, Brittany F.; Coyle, David R.; +5 more

Patterns of radiocesium contamination in eggs of free-ranging wood ducks

Journal Article · 1993 · Journal of Wildlife Management; (United States) · OSTI ID:5813710

Kennamer, R A; McCreedy, C D; Brisbin, Jr, I L

Raccoons (Procyon lotor) as Sentinels of Trace Element Contamination and Physiological Effects of Exposure to Coal Fly Ash

Journal Article · 2016 · Archives of Environmental Contamination and Toxicology · OSTI ID:1334824

Hernandez, Felipe; Oldenkamp, Ricki E.; Webster, Sarah; +3 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Inductively coupled plasma mass spectroscopy
Radiocesium
Radioecology
Savannah River Site
Scavenger beetles
Trace elements

Title: Bioaccumulation of contaminants in Scarabaeidae and Silphidae beetles at sites polluted by coal combustion residuals and radiocesium

Citation Formats

References (60)

Similar Records

Related Subjects