Abstract
Uranium is the heaviest naturally occurring element on Earth. Uranium mining may result in ground and surface water contamination with potential bioaccumulation and dispersion by aquatic invertebrates with aerial stages. We investigated the effects of uranium contamination at community level in terms of abundance, richness, the composition of invertebrate communities, and functional traits. We also investigated uranium mobility across aquatic food webs and its transfer to land via the emergence of aquatic insects. We sampled water, sediment, biofilm, macrophytes, aquatic invertebrates, adult insects, and spiders in the riparian zone across sites with a gradient of uranium concentrations in stream water (from 2.1 to 4.7 µg L−1) and sediments (from 10.4 to 41.8 µg g−1). Macroinvertebrate assemblages differed between sites with a higher diversity and predominance of Nemouridae and Baetidae at the reference site and low diversity and predominance of Chironomidae in sites with the highest uranium concentration. Uranium concentrations in producers and consumers increased linearly with uranium concentration in stream water and sediment (p < 0.05). The highest accumulation was found in litter (83.76 ± 5.42 µg g−1) and macrophytes (47.58 ± 6.93 µg g−1) in the most contaminated site. Uranium was highest in scrapers (14.30 ± 0.98 µg g−1), followed by shredders (12.96 ± 0.81 µg g−1) and engulfer predators (7.01 ± 1.3 µg g−1). Uranium in adults of aquatic insects in the riparian zone in all sites ranged from 0.25 to 2.90 µg g−1, whereas in spiders it ranged from 0.96 to 1.73 µg g−1, with no differences between sites (p > 0.05). There was a negative relationship between δ15N and uranium, suggesting there is no biomagnification along food webs. We concluded that uranium is accumulated by producers and consumers but not biomagnified nor dispersed to land with the emergence of aquatic insects.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00244-019-00677-y/MediaObjects/244_2019_677_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00244-019-00677-y/MediaObjects/244_2019_677_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00244-019-00677-y/MediaObjects/244_2019_677_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00244-019-00677-y/MediaObjects/244_2019_677_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00244-019-00677-y/MediaObjects/244_2019_677_Fig5_HTML.png)
Similar content being viewed by others
References
Ahsanullah M, Williams AR (1989) Kinetics of uranium uptake by the crab Pachygrapsus laevimanus and the zebra winkle Austrocochlea constricta. Mar Biol 327:323–327
Alam MS, Cheng T (2014) Uranium release from sediment to groundwater: influence of water chemistry and insights into release mechanisms. J Contam Hydrol 164:72–87. https://doi.org/10.1016/j.jconhyd.2014.06.001
Ali A-E, Sloane DR, Strezov V (2018) Assessment of impacts of coal mining in the region of Sydney, Australia on the aquatic environment using macroinvertebrates and chlorophyll as indicators. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph15071556
Amiard J, Geffard A, Amiard-Triquet C, Crouzet C (2007) Relationship between the lability of sediment-bound metals (Cd, Cu, Zn) and their bioaccumulation in benthic invertebrates. Estuar Coast Shelf Sci 72:511–521. https://doi.org/10.1016/j.ecss.2006.11.017
Ballan-Dufrançais C (2002) Localization of metals in cells of pterygote insects. Microsc Res Tech 56:403–420. https://doi.org/10.1002/jemt.10041
Bartrons M, Grimalt JO, Catalan J (2007) Concentration changes of organochlorine compounds and polybromodiphenyl ethers during metamorphosis of aquatic insects. Environ Sci Technol 41:6137–6141
Bergmann M, Sobral O, Graça MAS (in press) Activities of oxidative stress- and cell membrane-related enzymes in a freshwater leaf-shredder exposed to uranium. Limnetica
Bergmann M, Sobral O, Pratas J, Graça MAS (2018) Uranium toxicity to aquatic invertebrates: a laboratory assay. Environ Pollut 239:359–366. https://doi.org/10.1016/j.envpol.2018.04.007
Bleise A, Danesi PR, Burkart W (2003) Properties, use and health effects of depleted uranium (DU): a general overview. J Environ Radioact 64:93–112. https://doi.org/10.1016/S0265-931X(02)00041-3
Brooks AC, Gaskell PN, Maltby LL (2009) Importance of prey and predator feeding behaviors for trophic transfer and secondary poisoning. Environ Sci Technol 43:7916–7923
Carlisle DM, Clements WH (2003) Growth and secondary production of aquatic insects along a gradient of Zn contamination in Rocky Mountain streams. The University of Chicago Press on behalf of the Society for Freshwater. J N Am Benthol Soc 22:582–597
Cid N, Ibáñez C, Palanques A, Prat N (2010) Patterns of metal bioaccumulation in two filter-feeding macroinvertebrates: exposure distribution, inter-species differences and variability across developmental stages. Sci Total Environ 408:2795–2806. https://doi.org/10.1016/j.scitotenv.2010.03.030
Cole GA, Weihe PE (2016) Textbook of limnology, 5th edn. Waveland Press, Long Grove
Crawford SE, Lofts S, Liber K (2018) Predicting the bioavailability of sediment-bound uranium to the freshwater midge (Chironomus dilutus) using physicochemical properties. Environ Toxicol Chem 37:1146–1157. https://doi.org/10.1002/etc.4057
Cremona F, Hamelin S, Planas D, Lucotte M (2009) Sources of organic matter and methylmercury in littoral macroinvertebrates: a stable isotope approach. Biogeochemistry 94(1):81–94
Cremona F, Planas D, Lucotte M (2008) Assessing the importance of macroinvertebrate trophic dead ends in the lower transfer of methylmercury in littoral food webs. Can J Fish Aquat Sci 65:2043–2052. https://doi.org/10.1139/F08-116
Croteau M-N, Luoma SN, Stewart AR (2005) Trophic transfer of metals along freshwater food webs: evidence of cadmium biomagnification in nature. Limnol Ocean 50:1511–1519
Cui B, Zhang Q, Zhang K, Liu X, Zhang H (2011) Analyzing trophic transfer of heavy metals for food webs in the newly-formed wetlands of the Yellow River Delta, China. Environ Pollut 159:1297–1306. https://doi.org/10.1016/j.envpol.2011.01.024
Daley JM, Corkum LD, Drouillard KG (2011) Aquatic to terrestrial transfer of sediment associated persistent organic pollutants is enhanced by bioamplification processes. Environ Toxicol Chem 30:2167–2174. https://doi.org/10.1002/etc.608
Dias V, Vasseur C, Bonzom JM (2008) Exposure of Chironomus riparius larvae to uranium: effects on survival, development time, growth, and mouthpart deformities. Chemosphere 71:574–581
Edwards PG, Gaines KF, Bryan AL, Novak JM, Blas SA (2014) Trophic dynamics of U, Ni, Hg and other contaminants of potential concern on the Department of Energy’s Savannah River Site. Environ Monit Assess 186:481–500. https://doi.org/10.1007/s10661-013-3392-z
Einoder LD, MacLeod CK, Coughanowr C (2018) Metal and isotope analysis of bird feathers in a contaminated estuary reveals bioaccumulation, biomagnification, and potential toxic effects. Arch Environ Contam Toxicol 75:96–110. https://doi.org/10.1007/s00244-018-0532-z
Favas PJC, Pratas J, Mitra S, Sarkar SK, Venkatachalam P (2016) Biogeochemistry of uranium in the soil–plant and water–plant systems in an old uranium mine. Sci Total Environ 568:350–368. https://doi.org/10.1016/j.scitotenv.2016.06.024
Fisher NS, Hook SE (2002) Toxicology tests with aquatic animals need to consider the trophic transfer of metals. Toxicology 181–182:531–536. https://doi.org/10.1016/S0300-483X(02)00475-4
Fletcher DE, Lindell AH, Stillings GK, Blas SA, McArthur JV (2017) Trace element accumulation in lotic dragonfly nymphs: genus matters. PLoS ONE. https://doi.org/10.1371/journal.pone.0172016
Frelon S, Mounicou S, Lobinski R, Gilbin R, Simon O (2013) Subcellular fractionation and chemical speciation of uranium to elucidate its fate in gills and hepatopancreas of crayfish Procambarus clarkii. Chemosphere 91:481–490. https://doi.org/10.1016/j.chemosphere.2012.12.008
Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643. https://doi.org/10.1099/mic.0.037143-0
Hepp LU, Pratas JAMS, Graça MAS (2017) Arsenic in stream waters is bioaccumulated but neither biomagnified through food webs nor biodispersed to land. Ecotoxicol Environ Saf 139:132–138. https://doi.org/10.1016/j.ecoenv.2017.01.035
Hopkin SP, Martin MH (1985) Assimilation of zinc, cadmium, lead, copper, and iron by the spider Dysdera crocata, a predator of woodlice. Bull Environ Contam Toxicol 34:183–187
Howie MG, Jackson AK, Cristol DA (2018) Spatial extent of mercury contamination in birds and their prey on the floodplain of a contaminated river. Sci Total Environ 630:1446–1452. https://doi.org/10.1016/j.scitotenv.2018.02.272
INERIS (2008) Toxicological and environmental data sheets of chemicals. Inst Natl lénvironnement Ind. des risques. https://substances.ineris.fr/fr/substance/1887/3. Accessed 15 Apr 2018
Jha VN, Tripathi RM, Sethy NK, Sahoo SK (2016) Uptake of uranium by aquatic plants growing in fresh water ecosystem around uranium mill tailings pond at Jaduguda, India. Sci Total Environ 539:175–184. https://doi.org/10.1016/j.scitotenv.2015.08.120
Kaplan DI, Buettner SW, Li D, Huang S, Koster van Groos PG, Jaffé PR, Seaman JC (2017) In situ porewater uranium concentrations in a contaminated wetland: effect of seasons and sediment depth. Appl Geochem 85:128–136. https://doi.org/10.1016/j.apgeochem.2016.11.017
Kilgour BW, Dowsley B, McKee M, Mihok S (2018) Effects of uranium mining and milling on benthic invertebrate communities in the Athabasca Basin of Northern Saskatchewan. Can Water Resour J 43(3):305–320. https://doi.org/10.1080/07011784.2018.1445560
Kraemer LD, Evans D (2012) Uranium bioaccumulation in a freshwater ecosystem: impact of feeding ecology. Aquat Toxicol 124–125:163–170. https://doi.org/10.1016/j.aquatox.2012.08.012
Kraus JM, Walters DM, Wesner JS, Stricker CA, Schmidt TS, Zuellig RE (2014) Metamorphosis alters contaminants and chemical tracers in insects: implications for food webs. Environ Sci Technol. https://doi.org/10.1021/es502970b
Krawczyk-Bärsch E, Lünsdorf H, Pedersen K, Arnold T, Bok F, Steudtner R, Lehtinen A, Brendler V (2012) Immobilization of uranium in biofilm microorganisms exposed to groundwater seeps over granitic rock tunnel walls in Olkiluoto, Finland. Geochim Cosmochim Acta 96:94–104. https://doi.org/10.1016/j.gca.2012.08.012
Lagauzère S, Motelica-Heino M, Viollier E, Stora G, Bonzom JM (2014) Remobilisation of uranium from contaminated freshwater sediments by bioturbation. Biogeosciences 11:3381–3396. https://doi.org/10.5194/bg-11-3381-2014
Lavilla I, Rodríguez-Liñares G, Garrido J, Bendicho C (2010) A biogeochemical approach to understanding the accumulation patterns of trace elements in three species of dragonfly larvae: evaluation as biomonitors. J Environ Monit 12:724–730. https://doi.org/10.1039/b920379f
Lavoie RA, Jardine TD, Chumchal MM, Kidd KA, Campbell LM (2013) Biomagnification of mercury in aquatic food webs: a worldwide meta-analysis. Environ Sci Technol 47:13385–13394. https://doi.org/10.1021/es403103t
Li A, Zhou C, Liu Z, Xu X, Zhou Y, Zhou D, Tang Y, Ma F, Rittmann BE (2018a) Direct solid-state evidence of H2-induced partial U(VI) reduction concomitant with adsorption by extracellular polymeric substances (EPS). Biotechnol Bioeng 115:1685–1693. https://doi.org/10.1002/bit.26592
Li B, Chen F, Xu D, Wang Z, Tao M (2018b) Trophic interactions in the Zoige Alpine wetland on the eastern edge of the Qinghai-Tibetan Plateau inferred by stable isotopes. Limnology 19:285–297. https://doi.org/10.1007/s10201-018-0546-2
McKie BG, Sandin L, Carlson PE, Johnson RK (2018) Species traits reveal effects of land use, season and habitat on the potential subsidy of stream invertebrates to terrestrial food webs. Aquat Sci 80:1–12. https://doi.org/10.1007/s00027-018-0565-4
Mocq J, Hare L (2018) Influence of acid mine drainage, and its remediation, on lakewater quality and benthic invertebrate communities. Water Air Soil Pollut 229:28. https://doi.org/10.1007/s11270-017-3671-3
Mogren CL, von Kiparski GR, Parker DR, Trumble JT (2012) Survival, reproduction, and arsenic body burdens in Chironomus riparius exposed to arsenate and phosphate. Sci Total Environ 425:60–65. https://doi.org/10.1016/j.scitotenv.2012.03.009
Muscatello JR, Liber K (2009) Accumulation and chronic toxicity of uranium over different life stages of the aquatic invertebrate chironomus tentans. Arch Environ Contam Toxicol 57:531–539. https://doi.org/10.1007/s00244-009-9283-1
Naidoo S, Vosloo D, Schoeman MC (2013) Foraging at wastewater treatment works increases the potential for metal accumulation in an urban adapter, the banana bat (Neoromicia nana). Afr Zool 48(1):39–55. https://doi.org/10.3377/004.048.0111
Nakano S, Murakami M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. PNAS 98(1):166–170
Nentwig W, Blick T, Gloor D, Hanggi A, Christian K (2019) Araneae—spiders of Europe. http://www.araneae.unibe.ch/. Accessed 19 Jan 2019
Nie X, Dong F, Bian L et al (2017) Uranium binding on Landoltia punctata as a result of formation of insoluble nano-U (VI) and U (IV) phosphate minerals. ACS Sustain Chem Eng 5:1494–1502
O’Quinn GN (2005) Using terrestrial arthropods as receptor species to determine trophic transfer of heavy metals in a riparian ecosystem. Dissertation. University of Georgia
Overall RA, Parry DL (2004) The uptake of uranium by Eleocharis dulcis (Chinese water chestnut) in the Ranger Uranium Mine constructed wetland filter. Environ Pollut 132:307–320. https://doi.org/10.1016/j.envpol.2004.04.005
Paetzold A, Schubert CJ, Tockner K (2005) Aquatic terrestrial linkages along a braided-river: riparian arthropods feeding on aquatic insects. Ecosystems 8:748–759. https://doi.org/10.1007/s10021-005-0004-y
Piló D, Ben-hamadou R, Pereira F, Carric A, Pereira P, Corzo A, Gaspar MB, Carvalho S (2016) How functional traits of estuarine macrobenthic assemblages respond to metal contamination? Ecol Indic 71:645–659. https://doi.org/10.1016/j.ecolind.2016.07.019
Pinto MMSC, Silva MMVG, Neiva AMR (2004) Pollution of water and stream sediments associated with the Vale de Abrutiga uranium mine, Central Portugal. Mine Water Environ 23(2):66–75. https://doi.org/10.1007/s10230-004-0041-3
Punshon T, Gaines KF, Jenkins RA (2003) Bioavailability and trophic transfer of sediment-bound Ni and U in a southeastern wetland system. Arch Environ Contam Toxicol 44:30–35. https://doi.org/10.1007/s00244-002-1213-4
Quinn MR, Feng X, Folt CL, Chamberlain CP (2003) Analyzing trophic transfer of metals in stream food webs using nitrogen isotopes. Sci Total Environ 317:73–89. https://doi.org/10.1016/S0048-9697(02)00615-0
Rahman MA, Hasegawa H, Lim RP (2012) Bioaccumulation, biotransformation and trophic transfer of arsenic in the aquatic food chain. Environ Res 116:118–135. https://doi.org/10.1016/j.envres.2012.03.014
Rybak J, Rogula-kozłowska W, Loska K, Rutkowski R (2019) The concentration of Cu and Pb in the funnel spider Eratigena atrica (C. L. Koch 1843) (Araneae: Agelenidae) and its web. Chem Ecol 35:179–190. https://doi.org/10.1080/02757540.2018.1546295
Sanzone DM, Meyer JL, Marti E, Gardiner EP, Tank JL, Grimm NB (2003) Carbon and nitrogen transfer from a desert stream to riparian predators. Oecologia 134:238–250. https://doi.org/10.1007/s00442-002-1113-3
Schaller J, Brackhage C, Dudel EG (2011) Invertebrates minimize accumulation of metals and metalloids in contaminated environments. Water Air Soil Pollut 218:227–233. https://doi.org/10.1007/s11270-010-0637-0
Scheibener SA, Rivera NA, Hesterberg D, Duckworth OW, Buchwalter DB (2017) Elements 36:2991–2996. https://doi.org/10.1002/etc.3864
Sheppard SC, Sheppard MI, Gallerand MO, Sanipelli B (2005) Derivation of ecotoxicity thresholds for uranium. J Environ Radioact 79:55–83. https://doi.org/10.1016/j.jenvrad.2004.05.015
Simon O, Floriani M, Camilleri V, Gilbin R, Frelon S (2013) Relative importance of direct and trophic uranium exposures in the crayfish Orconectes limosus: implication for predicting uranium bioaccumulation and its associated toxicity. Environ Toxicol Chem 32:410–416. https://doi.org/10.1002/etc.2068
Solà C, Burgos M, Plazuelo Á, Toja J, Plans M, Prat N (2004) Heavy metal bioaccumulation and macroinvertebrate community changes in a Mediterranean stream affected by acid mine drainage and an accidental spill (Guadiamar River, SW Spain). Sci Total Environ 333:109–126. https://doi.org/10.1016/j.scitotenv.2004.05.011
Tachet H, Richoux P, Bournaud M, Usseglio-Polatera P (2000) Invertébrés D’ Eau Douce: systematique, biologie, écologie. CNRS Editions, Paris
Tagliaferro M, Gonçalves AMM, Bergman M, Sobral O, Graça MAS (2018) Assessment of metal exposure (uranium and copper) by the response of a set of integrated biomarkers in a stream shredder. Ecol Indic 95:991–1000. https://doi.org/10.1016/j.ecolind.2017.10.065
Van Loon Jon C, Barefoot RR (1989) Analytical methods for geochemical exploration. Academic Press, San Diego
Wesner JS, Walters DM, Schmidt TS, Kraus JM, Stricker CA, Clements WH, Wolf RE (2017) Metamorphosis affects metal concentrations and isotopic signatures in a mayfly (Baetis tricaudatus): implications for the aquatic-terrestrial transfer of metals. Environ Sci Technol 51(4):2438–2446
Wilczek G, Babczyńska A (2000) Heavy metals in the gonads and hepatopancreas of spiders (Araneae) from variously polluted areas. In: Gajdoš P, Pekár S (eds) Proceedings of the 18th European colloquium of arachnology. Ekológia (Bratislava), vol 19, Supplement 3, pp 283–292
Wood PJ, Hannah DM, Sadler JP (eds) (2007) Hydroecology and ecohydrology: past, present and future. Wiley, West Sussex
Acknowledgments
The authors thank Olimpia Sobral for field assistance and Luis Crespo for spider identification. This study was supported by the Portuguese Foundation for Science and Technology (FCT) through the strategic Project UID/MAR/04292/2013 granted to MARE. Melissa Bergmann was supported by the National Council for Technological and Scientific Development (CNPq) (GDE 206450/2014-1).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bergmann, M., Graça, M.A.S. Bioaccumulation and Dispersion of Uranium by Freshwater Organisms. Arch Environ Contam Toxicol 78, 254–266 (2020). https://doi.org/10.1007/s00244-019-00677-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00244-019-00677-y