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James Erdmann 25 November 2013

ZOO 4430 Limnology Dr. Lusha Tronstad

Term Paper: Impacts of Selenium on Aquatic Ecosystems Introduction Selenium (Se), atomic number 34 of the Periodic Table, is a trace element found naturally and ubiquitously on Earth at varying levels. The majority of Se on Earth resides in the crusts at low concentrations (0.05-0.09 parts per million; ppm) and at generally higher concentrations in derived igneous and sedimentary rocks and soils. These rock and soil concentrations, normally between 0.1 and 2 ppm, vary on a local to continental scale, as well as fluctuate from undetectably low to levels to concentrations over 100 ppm (Oldfield 2002, Fordyce 2013). Selenium has six naturally occurring isotopes and occurs in four oxidation states (Se2-, Se2+, Se4+, and Se6+), including elemental Se (Se0). The dominant forms of Se found on Earth are selenite (SeO32-) and selenate (SeO42-), depending on neighboring chemicals and the acidity and redox potential of the surrounding environment. In arid, alkaline regions, selenate is the dominant form of inorganic Se, while selenite is the dominant form in moist, acidic regions (Adriano 1986, Berrow and Ure 1989). Volcanic activity and rock weathering are the major natural sources of Se introduction into environments. In the past few hundred years, anthropogenic influences such as mining, metal processing, and fossil fuel burning have become important contributors of introduced Se (Fordyce 2013). Most forms of Se are water-soluble and easily taken up into organisms that consume them. The issue of Se poisoning in aquatic ecosystems is a relatively new one and has important conservation implications. The majority of previous work done on Se has looked at terrestrial toxicity in a variety of higher plants and animals. This knowledge, both inside and outside of limnology, can be used to safely remedy issues with Se around the world, and is being actively

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researched. The objective of my paper is to examine our current knowledge of the impacts of selenium (Se) on freshwater ecosystems, with a focus on trophic level influences. Mechanism of toxicity Selenium is an essential micronutrient to all animals and some prokaryotes, but has not yet been shown to be necessary for other eukaryotes such as plants and fungi (Stadtman 1996, Terry et al. 2000). However, Se can be problematic for all forms of life at either end of its environmental concentration spectrum. For those organisms that require Se, too little consumption (<0.010.1 dietary ppm) has severe consequences, including reduced fertility, cellular apoptosis, embryonic mortality and muscular dystrophy across animals, as well as osteoarthropathy, cancer, and thyroid dysfunction in humans (WHO 1987). Conversely, too much Se (>25 dietary ppm) has broad-scale negative impacts on life. Selenium toxicity or poisoning, termed selenosis, has been associated with animal diseases ranging from reproductive issues and developmental malformations, to alkali disease and blind stagger in ungulates, to various cancers, as well as plant diseases such as reduced growth, reduced pollen production, and chlorosis (de Souza et al. 1998, Prins et al. 2011, Fordyce 2013). This exceptionally narrow range between necessity and toxicity makes Se an important factor in ecosystem health. Normally, due to seleniums high chemical similarity to sulfur (S), Se in high enough concentrations can be non-specifically misincorporated into S-containing amino acids, replacing cysteine with selenocysteine and methionine with selenomethionine (WHO 1987, Sors et al. 2005). A clear consequence of altered amino acid composition is protein misfolding and altered activity, which causes proteins to lose proper function and has a plethora of cascading biological effects. These dysfunctional selenoproteins and other forms of Se tend to accumulate in the organisms, further escalating the impacts caused by the chemical (Fordyce 2013).

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Selenium in organisms Selenium is generally first taken up by plants and microbes and accumulates in organisms, subsequently bioaccumulating at increasing concentrations in higher trophic levels (Dallinger et al. 1987). However, some plants, algae, invertebrates and other organisms at lower levels on the food chain have evolved to bioaccumulate Se and other trace elements to levels toxic to their consumers, a mechanism to prevent predation known as the elemental defense hypothesis (Cherry and Guthrie 1977, Coleman et al. 2005). At lower levels in the food chain, Se is mainly taken up in inorganic forms originating directly from rocks and soils, whereas at higher trophic levels, Se intake is both organic and inorganic and mostly comes from food consumption. A critical factor in the amount of Se taken up and incorporated into cells by organisms, i.e. bioavailability, is the form of Se present. Selenate is normally the most bioavailable form of Se, followed by the seleno-amino acids, then by selenite, and finally elemental Se and selenide (Se2-; Fordyce 2013). Plants and algae are the main biological facilitators for introducing bioavailable Se, and can concentrate Se levels well over 1,000 times environmental concentrations within their cells (Ohlendorf 1989, Prins et al. 2011). Freshwaters contain minimal amounts of Se, rarely exceeding 0.01 ppm. Groundwaters normally contain higher levels of Se as a result of more rock-water interactions, with few reports of groundwaters having up to 1.0 ppm Se. Rarely occurring in nature, Se concentrations of up to 2.0 ppm have been reported in saline lakes (Fordyce 2013). The majority of Se in rivers is in particulate form and has little biological activity. Canton and others (1997) presented evidence that water Se concentrations alone are not adequate for predicting Se toxicity in aquatic organisms, and in fact is a poor predictor; accurately predicting toxicity is more closely associated with sediment Se concentrations. Lemly (1995) designed a protocol for assessing the

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degree of hazard Se has on an environment using weighted hazard values of five ecosystem components: water, sediments, benthic macroinvertebrates, fish eggs, and aquatic bird eggs. While aquatic animals can take up Se in the water directly from water through their gills, gut and epidermis, the majority still comes from dietary exposure, owing to their places in food webs (Dallinger et al. 1987). Selenium-sensitive aquatic species can reach lethal Se concentrations as low as 0.06 ppm in the water (Ohlendorf 1989). In terms of our understanding of Se impacts and movement, the base of the aquatic food chain, i.e. algae and higher aquatic plants, is a poorly studied trophic level. The majority of studies examining Se moving throughout aquatic ecosystems focus chiefly on animals (Hamilton 2004). In freshwater ecosystems with normal levels of Se, algae and plants generally contain between 0.1 and 2 ppm dry-weight Se. Algae are usually sensitive to Se concentration, reaching lethal levels before 1 ppm, although there is significant variation in Se tolerance among the members of this group (Eisler 1985). Some algae are able tolerate Se concentrations of over 30 ppm and are highly efficient at volatilizing it, while some algal species reach lethal Se levels well under 0.1 ppm (Eisler 1985, Huang et al. 2013). Algae and other aquatic microbes have also been found to preferentially take up selenite over short periods and uptake selenate gradually over their lifetimes (Riedel et al. 1996). The majority of Se bioaccumulation occurs at the base of the food web, the primary producers and consumers. In the next trophic levels, invertebrates, consisting of both primary and secondary consumers, are relatively poorly understood in their Se movement along the freshwater food chain. Zooplankton experimentally supplied with selenomethionine were found to bioconcentrate organic Se 200,000 times environmental levels (Lemly 1993a). Primary consumers are usually more sensitive to Se concentrations than secondary consumers and other

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macroinvertebrates. Daphnids bioconcentrate Se around 2,000 times environmental levels with lethal concentrations between 0.1 and 0.8 ppm, and a snails can bioconcentrate Se over 32,000 times environmental levels with lethal concentrations reached over 10 ppm. Daphnia magna showed reduced growth at concentrations as low as 0.156 ppm and reduced reproduction at water concentrations over 0.348 ppm (Ingersoll et al. 1990). In the same study, midges, Chironomus riparius, were only shown to have delayed emergence times at water Se concentrations over 0.837 ppm. Paramecium fed high-Se bacteria showed comparable Se levels as their food with no bioaccumulation (Sanders and Gilmour 1994). Vertebrates often dominate the higher trophic levels of aquatic ecosystems, creating concerns about their bioaccumulation of elements including Se. Selenium movement and accumulation within a vertebrates tissues is much more studied than within invertebrates, leading to greater knowledge of Se accumulation and settling (Fordyce 2013). The majority of work on freshwater ecosystem Se toxicity has been done on fish. In freshwater fish, Se accumulates most heavily in the liver, spleen, heart, and muscle, depending on the species and environmental Se concentration. Concentrations of up to 77.1 ppm fresh-weight have been observed in sunfish (Lepomis spp.), 36.2 ppm in catfish (Ictalurus spp.) and 36.7 ppm in carp (Cyprinus carpio), all correlated with high mortality and practically-absent reproduction from Se released by a connected steam station (Cumbie and Van Horn 1978). Extreme deformities and whole-body Se concentrations were observed in fish living in a lake containing 0.01 ppm Se in North Carolina, up to 130 times the concentrations found in nearby reference lakes (Lemly 1993b). Freshwater fish are generally more tolerant to Se than their trophic subordinates. Sensitive species can reach lethal Se concentrations below 1 ppm whereas many species can tolerate concentrations up to and over 10 ppm. A notably sensitive species, the rainbow trout, has

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anemia and reduced hatching rates at 0.05 ppm and reaches lethal Se concentrations at 0.06 ppm (Eisler 1985). On average across the United States, fish contain approximately 2 ppm dry-weight Se (Ohlendorf 1989). Dietary studies on fish have shown that taxa vary in sensitivity to selenium form, but they are most sensitive to selenomethionine before selenite and selenocysteine (Hamilton 2004). At the top of aquatic ecosystem food chains are often other vertebrates, namely birds. Aquatic avians have been carefully studied in multiple facets relating to Se toxicity, and have even become the poster child for the impacts of introduced Se. Birds are often indirectly highly sensitive to Se fluctuations. Birds consuming Se are not the most heavily impacted by the intake; the problem arises during egg development. Dietary Se intake of levels greater than 69 ppm is highly teratogenic to birds and can lead to embryonic mortality of 90% or more. Average dryweight Se concentrations in livers of birds from freshwater habitats range from 4 to 10 ppm, kidneys from 4 to 8 ppm, and eggs range from about 1 to 3 ppm dry-weight (Ohlendorf 1989). Currently, no significant work has been done on Se tolerance and toxicity in amphibians or reptiles (Peterson and Nebeker 1992). Two species of herptile collected from Kesterson Reservoir were found to have elevated Se tissue concentrations compared to nearby conspecifics, for example 45.0 ppm versus 6.22 ppm dry-weight from the livers of bullfrogs. However, the animals were not examined for signs of selenosis (Ohlendorf et al. 1988). Deformities and reduced survival were observed in tadpole eggs and larvae from water containing 0.002 ppm Se (Ohlendorf 1989). Many mammals have been studied for Se toxicity, but mainly in settings outside of aquatic environments, predominantly agriculture. In mammals, Se mainly bioaccumulates in the liver and kidneys and can be over 50 ppm dry-weight in the tissues of

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animals native to seleniferous environments without noted toxicity symptoms (Fordyce 2013). Herbivorous mammals generally contain < 2 ppm dry-weight in their livers Selenium deficiency in aquatic animals has been studied to a much lesser extent than toxicity, but it is still known to have negative effects on the growth, survival, and reproduction of fish, algae, mollusks, crustaceans, and other aquatic biota (Eisler 1985). A major factor in this research disequilibrium stems from the fact that a large portion of research originates from rapid ecosystem changes as a result of sudden introduction of Se through natural and anthropogenic actions. If there were a mechanism for the sudden removal of Se from an environment, this imbalance would likely not be so great. Case study Kesterson Reservoir is a major area of interest for examining the environmental effects of Se. Located in the San Joaquin Valley of California, Kesterson Reservoir receives water inputs from agricultural runoff. This runoff contains elevated levels of Se, which accumulates and evapoconcentrates in the reservoir. The impacts of high Se were first observed and reported in 1986 by Ohlendorf and others, who noticed significant hatchling deformities and embryonic mortality in coot and grebe birds nesting on the ponds receiving irrigation drainwater. Further investigation revealed the cause to be the elevated Se in the ponds. Some areas of Kesterson had sediment detritus Se concentrations of 440 ppm (Saiki and Lowe 1987). Clark (1987) found that mammals around the reservoir had significantly elevated levels of Se, but they did not show symptoms of selenosis. This area has been and continues to be a major contributor to the knowledge and awareness of the impacts of anthropogenic Se on multiple trophic, organismal, and ecological levels since the first report by Ohlendorf. Recently, Daz and colleagues (2013)

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tested the ability of six halophyte crop species to grow in the San Joaquin Valley and found that crop plants could be grown using the saline, seleniferous agricultural drainage water. Conclusions and future directions There is a tremendous amount of variation in the ability of organisms to tolerate Se levels both within and across trophic levels. The majority of this tolerance most likely comes from long-term adaptations to local Se concentrations. Unfortunately, human activities over the last few hundred years have led to rapid exposure of Se to environments with low natural concentrations around the globe. These cases often result in multi-species die-offs and local extinctions. It is improbable that the flora and fauna of these environments will be able to appropriately adapt to the new conditions, leading to the need for humans to intervene to prevent further damage than what weve already caused. Despite these environmental struggles, a lake tested for Se during and a decade after exposure from industrial activity was found to have significantly reduced Se concentrations; from 0.02 ppm in 1986 to <0.001 ppm in 1996 with an 8595% decrease in the Se of the lakes biota, an example of the environment rebounding, at least chemically. (Lemly 1997). Over the past few years, researchers have been attempting to address the problems of Se deficiency and toxicity in environments. Eliminating these unhealthy Se levels by natural means is a priority for conservation of local biology and biodiversity. While the majority of this work has focused on terrestrial remediation, the concepts remain the same. The major focus of rehabilitating these ecosystems is through phytoremediation, or using plants to remedy or reverse environmental damage. Several species of vascular plants in selected taxa are able to accumulate Se at concentrations hundreds to thousands of times above what is present in the environment. These plants, called selenium-accumulators and hyperaccumulators, are able to take up organic

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and inorganic Se and convert it to a methylated organic form of selenium, which is highly volatile and is released into the atmosphere (Mehdawi and Pilon-Smits 2011). This method of remediation is currently being investigated for aquatic plants such as cattail, Elodea, duckweed, Azolla, and water hyacinth, species known to be tolerant to Se (Pilon-Smits 2005). Huang and others (2013) proposed a method of Se treatment using a combination of an algal pre-treatment field followed by a cattail wetland system to purify water downstream of a seleniferous water source, creating a Species Conservation Habitat. To my knowledge, this model has yet to be employed, but has a very sound design. Gerhardt and others (1991) designed a method of Se removal using algae to accumulate Se, then placing them in anoxic containers with bacteria, which consumed the algae and reduced the Se to less bioavailable, insoluble forms that could be manually removed and properly disposed of. This model was later tested and found to work moderately well (Amweg et al 2003). It will likely be years before any large-scale plans for aquatic Se phytoremediation are implemented, but great strides have been made in the past two decades regarding the subject. As we continue exploring the mechanisms of selenium accumulation and volatilization across trophic levels in aquatic ecosystems, and searching for organisms that can be utilized for remediation of Se, we will most certainly encounter both new and beneficial aids, as well as roadblocks and unexpected, unintended results. Similar to these methods, Se accumulator plants may be used in Se-deficient environments to better collect what little Se is available and make it more accessible to the surrounding organisms (Bauelos et al. 2012). Selenium plays a critical role in aquatic ecosystems around the globe. While Se deficiency is still poorly studied, Se toxicity, a prevalent and growing issue in many areas of the world, is better understood and being actively researched with various remediation methods.

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Anthropogenic origins of Se in aquatic systems have had severe consequences resulting in dieoffs throughout the aquatic food web and beyond. In general, Se concentration and tolerance increases through higher trophic levels, but there is significant variation within a given level, with the majority of variation and initial accumulation existing at the base of the food chain. There is much more to be learned about the trophic and environmental interactions selenium has on aquatic ecosystems, but we have a strong scientific foundation that can be used to further knowledge and reclamation practices. Literature Cited Adriano, D.C. 1986. Trace elements in the terrestrial environment. Springer-Verlag, New York, New York. Amweg, E.L., D.L. Stuart, and D.P. Weston. 2003. Comparative bioavailability of selenium to aquatic organisms after biological treatment of agricultural drainage water. Aquatic Toxicology 63: 1325. Bauelos, G.S., C. Stushnoff, S.S. Walse, T. Zuber, S.I. Yang, I.J. Pickering, and J.L. Freeman. 2012. Biofortified, selenium enriched, fruit and cladode from three Opuntia cactus pear cultivars grown on agricultural drainage sediment for use in nutraceutical foods. Food Chemistry 135: 916. Berrow, M.L., and A.M. Ure. 1989. Geological materials and soils. Pages 213242 in M. Ihnat, editor. Occurrence and distribution of selenium. CRC Press, Boca Raton, Florida. Cherry, D.S., and R.K. Guthrie. 1977. Toxic metals in surface waters from coal ash. Journal of the American Water Resources Association 13: 12271236. Clark, D.R. 1987. Selenium accumulation in mammals exposed to contaminated California irrigation drainwater. The Science of the Total Environment 66: 147168.

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Coleman, C.M., R.S. Boyd, and M.D. Eubanks. 2005. Extending the elemental defense hypothesis: dietary metal concentrations below hyperaccumulator levels could harm herbivores. Journal of Chemical Ecology 31: 16691681. Cumbie, P.M., and S.L. Van Horn. 1978. Selenium accumulation associated with fish mortality and reproductive failure. Proceedings of the Annual Conference Southeastern Association of Fish and Wildlife Agencies 32: 612624. Dallinger, R., F. Prosi, H. Segner, and H. Back. 1987. Contaminated food and uptake of heavy metals by fish: a review and a proposal for further research. Oecologia 73: 9198. Daz, F.J., S.E. Benes, and S.R. Grattan. 2013. Field performance of halophytic species under irrigation with saline drainage water in the San Joaquin Valley of California. Agricultural Water Management 118: 5969. Eisler R. 1985. Selenium hazards to fish, wildlife and invertebrates: a synoptic review. U.S. Fish and Wildlife Service Biological Report 85 (1.5). Fordyce, F.M. 2013. Selenium deficiency and toxicity in the environment. Pages 375416 in O. Senilus, et al., editors. Essentials of medical geology: revised edition. British Geological Survey, Nottingham. Gerhardt, M.B., F.B. Green, R.D. Newman, T.J. Lundquist, R.B. Tresan, and W.J. Oswald. 1991. Removal of selenium using a novel algal-bacterial process. Research Journal of The Water Pollution Control Federation 63: 799805. Hamilton, S.J. 2004. Review of selenium toxicity in the aquatic food chain. Science of The Total Environment 326: 131.

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Huang, J.-C., M.C. Surez, S.I. Yang, Z.-Q. Lin, and N. Terry. 2013. Development of a constructed wetland water treatment system for selenium removal: incorporation of an algal treatment component. Environmental Science and Technology 47: 1051810525. Ingersoll, C.G., F.J. Dwyer, and T.W. May. 1990. Toxicity of inorganic and organic selenium to Daphnia magna (Cladocera) and Chironomus riparius (Diptera). Environmental Toxicology and Chemistry 9: 11711181. Lemly, A.D. 1993a. Guidelines for evaluating selenium data from aquatic monitoring and assessment studies. Environmental Monitoring and Assessment 28: 83100. Lemly, A.D. 1993b. Teratogenic effects of selenium in natural populations of freshwater fish. Ecotoxicology and Environmental Safety 26: 181204. Lemly, A.D. 1995. A protocol for aquatic hazard assessment of selenium. Ecotoxicology and Environmental Safety 32: 280288. Lemly, A.D. 1997. Ecosystem recovery following selenium contamination in a freshwater reservoir. Ecotoxicology and Environmental Safety 36: 275281. Mehdawi, El, A.F., and E.A.H. Pilon-Smits. 2011. Ecological aspects of plant selenium hyperaccumulation. Plant Biology 14: 110. Oldfield, J.E. 2002. Selenium world atlas: updated edition. Selenium-Tellurium Development Association. Grimbergen, Belgium. Ohlendorf, H.M. 1989. Bioaccumulation and effects of selenium in wildlife. Pages 133177 in L.W. Jacobs, editor. Selenium in agriculture and the environment. Soil Science Society of America, Davis, California. Ohlendorf, H.M., R.L. Hothem, and T.W. Aldrich. 1988. Bioaccumulation of selenium by snakes and frogs in the San Joaquin Valley, California. Copeia 1988: 704710.

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Ohlendorf, H.M., D.J. Hoffman, M.K. Saiki, and T.W. Aldrich. 1986. Embryonic mortality and abnormalities of aquatic birds: apparent impacts of selenium from irrigation drainwater. The Science of the Total Environment 52: 4963. Peterson, J.A., and A.V. Nebeker. 1992. Estimation of waterborne selenium concentrations that are toxicity thresholds for wildlife. Archives of Environmental Contamination and Toxicology 23: 154162. Pilon-Smits, E.A.H. 2005. Phytoremediation. Plant Biology 56: 1539. Prins, C.N., L.J. Hantzis, C.F. Quinn, and E.A.H. Pilon-Smits. 2011. Effects of selenium accumulation on reproductive functions in Brassica juncea and Stanleya pinnata. Journal of Experimental Botany 62: 56335640. Ranjard, L., S. Nazaret, and B. Cournoyer. 2003. Freshwater bacteria can methylate selenium through the thiopurine methyltransferase pathway. Applied and Environmental Microbiology 69: 37843790. Riedel, G.F., J.G. Sanders, and C.C. Gilmour. 1996. Uptake, transformation, and impact of selenium in freshwater phytoplankton and bacterioplankton communities. Aquatic Microbial Ecology 11: 4351. Saiki, M.K., and T.P. Lowe. 1987. Selenium in aquatic organisms from subsurface agricultural drainage water, San Joaquin Valley, California. Archives of Environmental Contamination and Toxicology 16: 657670. Sanders, R.W., and C.C. Gilmour. 1994. Accumulation of selenium in a model freshwater microbial food web. Applied and Environmental Microbiology 60: 26772683. Sors, T.G., D.R. Ellis, and D.E. Salt. 2005. Selenium uptake, translocation, assimilation and metabolic fate in plants. Photosynthesis Research 86: 373389.

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de Souza MP, E. Pilon-Smits, C. Lytle, S. Hwang, J. Tai, T. Honma, L. Yeh, and N. Terry. 1998. Rate-limiting steps in selenium assimilation and volatilization by Indian mustard. Plant Physiology 117: 14871494. Stadtman, T.C. 1996. Selenocysteine. Annual Review of Biochemistry 65: 83100. Terry, N., A.M. Zayed, M.P. de Souza, and A.S. Tarun. 2000. Selenium in higher plants. Annual Review of Plant Biology 51: 401432. World Health Organization. 1987. Environmental health criterion 58selenium. World Health Organization, Geneva, Switzerland.

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