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Bioaccumulation dynamics of arsenate at the base of aquatic food webs Adeline R. Lopez, Dean R. Hesterberg, David H. Funk, and David B Buchwalter Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b01453 • Publication Date (Web): 25 May 2016 Downloaded from http://pubs.acs.org on May 28, 2016
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Bioaccumulation dynamics of arsenate at the base of aquatic food webs Adeline R. Lopez1, Dean R. Hesterberg2, David H. Funk3, David B. Buchwalter4* 1
Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina
27695, United States 2
Department of Soil Science, North Carolina State University, Raleigh, North Carolina 27695,
United States 3
Stroud Water Research Center, Avondale, Pennsylvania 19311, United States
4
Department of Environmental and Molecular Toxicology, North Carolina State University,
Raleigh, North Carolina, 27695, United States *Corresponding author phone: 919-513-1129; fax: 919-515-7169; email:
[email protected]. KEYWORDS Arsenic Bioaccumulation Periphyton Mayfly
1 2 3 4 5 6 7 8 9
ABSTRACT. Periphyton is an important food source at the base of freshwater ecosystems that tends to bioconcentrate trace elements making them trophically available. The potential for arsenic–a trace element of particular concern due to its widespread occurrence, toxicity and carcinogenicity–to bioconcentrate in periphyton and thus be available to benthic grazers is less well characterized. To better understand arsenate bioaccumulation dynamics in lotic food webs we used a radiotracer approach to characterize accumulation in periphyton and subsequent trophic transfer to benthic grazers. Periphyton bioconcentrated As between 3,200–9,700-fold (dry weight) over 8 days without reaching steady state, suggesting that periphyton is a major sink for arsenate. However, As-enriched periphyton as a food source for the mayfly Neocloeon 1
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triangulifer resulted in negligible As accumulation in a full lifecycle exposure. Additional studies estimate dietary assimilation efficiency in several primary consumers ranging from 22% in the mayfly N. triangulifer to 75% in the mayfly Isonychia sp.. X-ray fluorescence mapping revealed that As was predominantly associated with iron oxides in periphyton. We speculate that As adsorption to Fe in periphyton may play a role in reducing dietary bioavailability. Together these results suggest that trophic movement of As in lotic food webs is relatively low, though species differences in bioaccumulation patterns are important.
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Introduction:
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A growing body of literature highlights the importance of bioaccumulation of potentially toxic
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trace elements at the base of freshwater food webs (e.g.,1–4) and the importance of dietary
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exposure routes in dictating accumulation.5 Periphytic biofilms comprise different types of
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diatoms, algae, bacteria, fungi, and detritus that are often the predominant food resource at the
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base of aquatic food webs. Periphyton can significantly bioconcentrate trace elements and act as
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a dietary vector for metal exposures to grazing fauna. For example, cadmium,6,7 zinc,8 copper,4
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and selenium9,10 have all been shown to accumulate in periphytic biofilms and are trophically
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transferred to invertebrate grazers. In contrast, less is known about periphytic uptake,
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bioconcentration, and trophic transfer of arsenic.
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Arsenic is the 20th most abundant element in the Earth’s crust,11 and is a common contaminant
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in aquatic ecosystems as well as an EPA priority pollutant.12 The mineral co-localization of As
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with geologic resources such as metal rich ores and coal often result in As contamination
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associated with the extraction and use of these natural resources (e.g. mining, smelting, and coal
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combustion). Background concentrations of As in rivers are reported to range from 0.02 µg L-1
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to 2 µg L-1, while contaminated rivers typically range from 1-280 µg L-1 but have been reported
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as high as 79,000 µg L-1.13 While arsenate is expected to be the thermodynamically favored
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chemical species of As in oxic lotic systems,13 the biogeochemistry of As is complex, as it can
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exists in different oxidation states in the environment (-3, 0. +3, and +5) depending on redox 2
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conditions and pH.13 This speciation is further complicated by the fact that As can be converted
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biologically to several organic forms13,14 or converted between inorganic oxidation states
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(e.g.,15,16). These chemical forms dictate how As behaves in the environment and its potential to
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cause toxicity.17,18 For example, while arsenate is generally considered to be less mobile in the
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aquatic environment and less toxic than arsenite (the As species favored under reducing
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conditions such as in streambed sediments)18, environmental conditions (e.g., redox) or
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biological organisms can alter the chemical speciation of arsenate such that it becomes more
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(reduction to arsenite) or less (methylation) toxic. Less is understood about the dynamics of As
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at the base of freshwater food webs, particularly with respect to accumulation into periphytic
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biofilms and its availability to invertebrate grazers.
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Field studies indicate that As accumulation in periphytic biofilms is potentially important since
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measured concentrations have been shown to exceed those for water or sediment (e.g.,19–21).
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Similar observations have been reported for algae,21,22 bryophytes,23 and aquatic plants,24 though
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the complexity and variability in natural systems complicates quantifying accumulation
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dynamics for As. Laboratory studies similarly demonstrate that As is accumulative in a variety of
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aquatic plants (e.g.,25–27), algae (e.g.,25–27), and bacteria.26,28 While this accumulation is highly
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variable27,29,30 several species are such strong As accumulators that they have been proposed for
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use in As bioremediation.29–32 In comparison to these single-species evaluations, much less is
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known about the accumulation dynamics of As in environmentally realistic and complex
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assemblages of periphyton.
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Accumulation of As by primary producers at the base of the food web may have important
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implications for trophic transfer. Field studies report that tissue concentrations of As in
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organisms are better correlated with the concentration in their food than with water.33 Dietary 3
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exposure has also been suggested to drive As accumulation in several laboratory studies. For
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example Maeda34 found that benthic grazers accumulated an order of magnitude greater As from
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food than from water, and Williams et al.35 reported that ingested microalgae could be
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responsible for more than 80% of accumulated As inLeptrocheirus plumulosus. Slightly lower
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dietary contributions of 30–60% in Arenicola marina were reported by Casado-Martinez et al.,36
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but this was still an important pathway of accumulation. While aqueous exposure may also
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contribute to As accumulation (e.g.,37), these findings along with observations for other trace
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elements4,6–9 suggest that trophic transfer of As from primary producers to primary consumers is
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important and needs to be better characterized across a broader range of benthic grazers.
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In this study we used a radiotracer approach to quantitate the bioconcentration of arsenate (the
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As species dominating lotic systems) by natural periphyton assemblages at environmentally
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realistic concentrations. Lab-reared parthenogenetic Neocloeon triangulifer larvae were then
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raised on these differentially contaminated diets for a full life cycle experiment to investigate
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trophic transfer. These dietary bioaccumulation studies were combined with assays that
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examined As assimilation efficiency from food in a variety of benthic invertebrates, and
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microprobe analysis of As in periphyton to better understand As accumulation dynamics at the
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base of the aquatic food web.
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Methods:
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Reagents:
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Arsenate (HAsNa2O4●7H2O) was obtained from Alfa Aesar (MA, USA).
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As was obtained
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from the National Isotope Development Center (U.S. Dept. of Energy) as As(V) in 0.1 M HCl.
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Working secondary stock solutions were prepared in 0.1 N Omnitrace™ nitric acid (EMD
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Chemicals, Darmstadt, Germany). American Society for Testing and Materials (ASTM) artificial 4
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soft water (ASW) (mM: 0.57 NaHCO3, 0.17 CaSO4*2H2O, 0.25 MgSO4, and 0.03 KCl) was
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also used for all experiments.
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Test animals:
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N. triangulifer (WCC-2 clone originally obtained from culture at Stroud Water Research
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Center [SWRC], Avondale, PA) were reared in the lab at room temperature with ambient light.
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Other larval insects and benthic invertebrates were field collected from the Eno River (Efland,
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NC and Durham, NC) and Basin Creek (Sparta, NC), and allowed to acclimate without food for
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at least 48 hours to the laboratory cold room (approximately 15°C).
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Natural periphyton communities:
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Natural periphyton assemblages were obtained from SWRC, where they were cultivated by
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allowing fresh water from White Clay Creek, PA to flow over acrylic plates (6.5 x 23 x 0.15 cm;
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see supplemental table 1 for historical taxonomic data). Periphyton plates were shipped
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overnight on ice and were subsequently aerated and held at room temperature until experimental
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use. Background concentrations of As in periphyton (4.5±1.2 mg kg-1 dry wt) were determined
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using nitric acid digestion and Elan DRCII ICP-MS (PerkiniElmer, Waltham, MA; MDL
