Influence of Metal Contamination and Sediment Deposition on Benthic

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Ecotoxicology and Human Environmental Health

INFLUENCE OF METAL CONTAMINATION AND SEDIMENT DEPOSITION ON BENTHIC INVERTEBRATE COLONIZATION AT THE NORTH FORK CLEAR CREEK SUPERFUND SITE, COLORADO, USA Brittanie L. Dabney, William H Clements, Jacob L Williamson, and James F. Ranville Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b06556 • Publication Date (Web): 29 May 2018 Downloaded from http://pubs.acs.org on May 30, 2018

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Environmental Science & Technology

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Title: Influence of metal contamination and sediment deposition on benthic invertebrate

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colonization at the North Fork Clear Creek superfund site, Colorado, USA

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Authors: Brittanie L. Dabney1*, William H. Clements1, Jacob L. Williamson2, James F.

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Ranville2

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Affiliations: 1Department of Fish, Wildlife, and Conservation Biology, Colorado State

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University, Fort Collins, Colorado 80523, USA, 2Department of Chemistry and

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Geochemistry, Colorado School of Mines, Golden, Colorado 80401, USA

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Corresponding Author: Brittanie L. Dabney

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Department of Environmental Toxicology,

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Texas Tech University, Lubbock, TX 79409.

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Email: [email protected]

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ORCID: 0000-0002-7100-7600

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TOC/Abstract Graphic

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ABSTRACT Assessing benthic invertebrate community responses to multiple stressors is

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necessary to improve the success of restoration and biomonitoring projects. Results of

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mesocosm and field experiments were integrated to predict how benthic

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macroinvertebrate communities would recover following the removal of acid mine

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drainage from the North Fork of Clear Creek (NFCC), a U.S. EPA Superfund site in

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Colorado, USA. We transferred reference and metal-contaminated sediment to an

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upstream reference site where colonization by benthic macroinvertebrates was

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measured over 30 days. Additionally, a mesocosm experiment was performed to test

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the hypothesis that patches of metal-contaminated substrate impede recolonization

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downstream. Abundance in all treatments increased over time during field experiments;

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however, colonization was slower in treatments with metal-contaminated fine sediment.

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Community assemblages in treatments with metal-contaminated fine substrate were

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significantly different from other treatments. Patterns in the mesocosm study were

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consistent with results of the field experiment and showed greater separation in

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community structure between streams with metal-contaminated sediments and

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reference-coarse habitats; however, biological traits also helped explain downstream

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colonization. This study suggests that after water quality improvements at NFCC, fine-

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sediment deposition will likely reduce recovery potential for some taxa; however highly

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mobile taxa that avoid patches of contaminated habitats can recover quickly.

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INTRODUCTION Fine sediment and low amounts of trace metals occur naturally in aquatic

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ecosystems; however, human activities increase these inputs and result in low

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abundances of aquatic organisms at sites affected by mining activities.1–4 Mining can

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contribute to fine sediment deposition in aquatic ecosystems resulting in habitat loss,

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streambed homogenization, contaminant-loading and alterations of ecosystem

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functions, each of which impacts aquatic organisms.4–7 Independent of metal

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contamination, accumulation of sediment particles < 2 mm is often associated with the

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physical stress by abrasion and disruption of benthic invertebrate community

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structure.8–11 As the release of metals and sediment from historical and modern mining

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activities continues to degrade aquatic ecosystems, restoration managers require

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information on macroinvertebrate community responses if they hope to improve the

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likelihood of success in restoring mined watersheds.

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Research on the combined effects of metals and fine sediment on aquatic

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macroinvertebrates has mostly focused on single-species laboratory tests and

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observational studies. Observational studies show low benthic invertebrate

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abundances at sites with metal contamination.12,13 However, similar community

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responses to fine sediment accumulation have been reported from field experimental

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and observational studies.14,15 Laboratory studies show metal-contaminated fine-

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sediment can inhibit growth of invertebrates,16 reduce fertility,17 and that metals

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bioaccumulate in organisms.10,18,19 Exposure to metals in the sediment may also be

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higher compared to aqueous-only exposures depending on feeding strategy and

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behavioral aviodance.20–22 Benthic invertebrates may ingest metal-contaminated fine

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sediments, thereby increasing body burdens of metals.23,24 Macroinvertebrates may

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also avoid metal-contaminated sediment, thus reducing likelihood of exposure.21,22,25

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These species-specific factors may result in an over- or underestimation of the impacts

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of metal-contaminated fine sediment on recovery of mining-impacted streams. Field and

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mesocosm experiments can be useful in determining cause-and-effect relationships at

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sites with multiple stressors, and many authors have recognized the importance of

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incorporating experimentation in applied studies.7,13,26,27 However, field experiments

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that test the combined effects of both metal-contamination and fine-sediment deposition

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on benthic invertebrate community responses have not received much attention, even

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though these stressors often co-occur in mining-impacted watersheds.

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Several studies have found that high sediment inputs at mining sites exceed the

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input produced from natural landscapes.28–30 Metal contaminated sediments can

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remain in aquatic ecosystems long after the source of contamination has been

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eliminated,31 thereby increasing the duration of metal exposure, with long-term

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implications on stream health. This can be especially detrimental in the Rocky

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Mountain streams where most species are adapted to cobble and gravel-bed habitats

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that provide enough interstitial space for refuge. A loss of macroinvertebrate habitat

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due to clogging of interstitial spaces can have impacts on species abundance and

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distributions in streams.4,32

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The ability of macroinvertebrates to recolonize previously disturbed areas has

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been demonstrated,33 but field experiments to determine cause-and-effect relationships

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are lacking. Understanding how macroinvertebrates respond following a disturbance is

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especially important in stream restoration projects and estimating recovery potential.34



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Additionally, behavioral avoidance of contaminated sediments, which has been

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understudied in macroinvertebrate communities, can provide a more environmentally

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realistic assessment of ecological responses to stressors.35 This study used an

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experimental approach to quantify the combined effects of metal contamination and fine

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sediment deposition on benthic invertebrate communities. We performed a field

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experiment with the objective of predicting responses of benthic invertebrate

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communities after remediation of the North Fork Clear Creek (NFCC), a U.S. EPA

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Superfund site impacted by both metal contamination and fine sediment deposition.

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Environmental stressors may increase the patchiness of benthic invertebrate

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populations in lotic environments and influence populations colonizing downstream

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reaches.36,37 There is also evidence that benthic invertebrates exhibit avoidance

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behavior when exposed to metals and that avoidance is a highly sensitive indicator of

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environmental stress.35 Therefore, a mesocosm experiment was conducted to test the

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hypothesis that contaminated habitats influence downstream colonization, and the

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likelihood of benthic invertebrate movement beyond patches of contaminated sediment.

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Since previous research has shown that feeding strategies and mobility traits may

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influence sensitivity or exposure to metals,20,38 we also examined whether trait

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responses influenced downstream colonization in our mesocosm experiment. These

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research objectives were designed to help predict recovery at the NFCC following

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improvements in water quality, but also to answer broader ecological questions about

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the effects of multiple stressors on the distribution and recruitment of

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macroinvertebrates in restored streams.


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MATERIALS AND METHODS

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Study Site: The colonization experiment was performed at a reference site

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upstream of metal contamination in the North Fork of Clear Creek (NFCC; N39.81271,

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W105.49821) in Blackhawk, Colorado, USA in (Figure S1). NFCC is a tributary to the

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Clear Creek watershed and located approximately 50 km west of Denver, Colorado,

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USA. The downstream reach on NFCC was designated a U.S. Environmental

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Protection Agency (EPA) Superfund site in 1983 due to elevated levels of metals. High

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concentrations of zinc, cadmium, copper, iron and aluminum39 have resulted in low

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benthic invertebrate abundances and there are no fish populations present. Clear

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Creek is used for drinking water, local industry, and recreational purposes, making the

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water quality issues on NFCC a serious human health concern. Construction of a water

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treatment plant on NFCC was initiated and became operational in early 2017. Due to

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previous mining activities, NFCC has been severely degraded by both acid mine

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drainage from a point source and fine sediment accumulation from various non-point

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sources. Steep incline of the streambanks, tailings piles in the riparian areas, and the

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close proximity to a road makes NFCC highly susceptible to sediment accumulation

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from mining and other anthropogenic activities.

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Field Experiment: The colonization experiment was performed upstream of the

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source of mining contamination at a reference site from August to September 2014.

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Physicochemical characteristics of the reference site were monitored throughout the

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project with YSI meters (models 550A and 63; YSI Incorporated, Yellow Springs, OH),

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with an average ± standard deviation (SD) of water temperature of 8.16 ± 3.06 °C,



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dissolved oxygen of 9.18 ± 0.78 mg/L, and pH of 7.86 ± 0.15. Unlike sites downstream

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of the contamination, habitat at the reference site is a heterogeneous mixture of riffles

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and pools. The high diversity of benthic invertebrates and presence of fish populations

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at the reference site are the targeted restoration goals for the downstream reaches.

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Because recolonization of the downstream reaches will occur predominantly from

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macroinvertebrate drift, it is important to understand how this community will respond to

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stressors.

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Metal contaminated sediments were collected in NFCC near the source of

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contamination (N39.79867, W105.48174) and moved 2.6 km upstream to the reference

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site (Figure S1). At both the reference and metal contaminated sites, areas of sediment

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deposition were located, and fine sediment was collected from the stream. The

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experiment used six treatments in a full factorial design to discern between the impacts

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of metal contamination and sediment deposition (Figure 1a). Treatments were created

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by placing coarse sediment (i.e. cobble > 2360 µm) from the metal contaminated or

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reference site in colonization trays (25 x 25 x 10 cm). In addition to the coarse

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sediment, these colonization trays were either filled with fine-sediment (i.e. sand/silt

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50% of the dissimilarity between treatments and tray positions in the PERMANOVA

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tests.48

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Mobility and ecology traits were assessed based on a comprehensive trait

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dataset,49 which was obtained from the literature. We analyzed four groups of

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functional traits: drift frequency (abundance, common, and rare drift frequency);

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swimming ability (none, weak, and strong swimmers); habitat preference (burrow, climb,

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crawl, sprawl, and swim habitat) and feeding guild (collector-gatherer, collector-filterer,

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herbivore, predator, and shredder). Using a factorial design, relationships among fine



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sediment, metal contamination, tray (source, treatment, and sink trays) and

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macroinvertebrate communities were examined. For trait comparisons, only treatments

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A (reference-coarse sediment) and F (metal-contaminated coarse and fine sediment)

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were compared to determine if patches of metal-contaminated sediment present at

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NFCC could affect the type of invertebrates that colonize downstream suitable habitats.

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A two-way PERMANOVA was performed to test effects of treatment (A vs. F; Figure 1a)

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and tray position (source, treatment, and sink; Figure 1c).

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RESULTS Field Colonization Experiment: Iron, zinc, manganese, copper and nickel were

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the dominant metals measured on NFCC substrate, and concentrations of these metals

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were combined to estimate threshold effect concentrations. Metal concentrations in the

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trays were not significantly different throughout the experiment and concentrations in

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the metal treatments approximated values measured at our metal-contaminated

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collection site.38,50 Total metal concentrations in treatments with reference-site coarse

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substrate (RC) remained significantly lower than in treatments with metal-contaminated

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coarse and fine sediment (F = 10.1, p = 0.0002; Table S1). Additionally, the amount of

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fine sediment in each treatment did not significantly change over time (p > 0.05), and

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NF (no fines) trays had significantly less fine sediment than RF (reference fines) and MF

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(metal fines) trays (p < 0.01; Table S2). Organic matter in treatments was relatively

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constant throughout the experiment (Table S2). DISTLM analysis showed that organic

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matter was the most important variable influencing macroinvertebrate trends in all

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treatments expect for trays with metal coarse and fines (Table S3).


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Over 24,000 insects distributed among 37 genera were collected and identified

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during this experiment. PROC GLM results showed varying responses of total

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abundance, number of taxa, and diversity to metal contamination and sediment

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deposition with no three-way interaction between fines, metals, and day (Figure 2; Table

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S4). Total benthic invertebrate abundance increased over time in all treatments but was

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significantly lower in metal treatments compared to reference sediment. The effect of

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metal contamination on total abundance decreased over time, as indicated by the

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significant metals x day interaction term. In contrast, the impact of fine sediment

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appeared to increase over time between treatments with NF and MF. On day 30,

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treatments with reference coarse-sediment and reference-fines declined.

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Of the 37 taxa collected during this experiment, Baetis sp. (Ephemeroptera),

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Taenionema pallidum (Plecoptera), Rhyacophila sp. (Trichoptera), and Chironomidae

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(Diptera) were the most dominant in their corresponding insect orders. The responses

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of these dominant taxa to metal contamination were similar to those observed for total

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abundance; however, each taxon had a varying response to fine sediment deposition

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(Figure 2). The dominant mayfly (Baetis sp.) was not significantly affected by fine

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sediment (p = 0.1906), whereas abundance of the stonefly T. pallidum was greatest in

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treatments with only coarse sediment. Abundance of the caddisfly Rhyacophila sp. was

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also significantly lower on metal contaminated fine sediment compared to the other

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treatments. Chironomidae responded negatively to fine-sediment deposition; however,

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specific responses to metal-contaminated fines were variable throughout the

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experiment.



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Results of multivariate analysis showed that community assemblages

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significantly responded to fine sediment and metal contamination, and that these results

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varied over time (Figure 3; Table 1). Similar to responses of dominant taxa, community

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assemblages showed significant responses to fine-sediment (p = 0.009) and metal

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contamination (p = 0.001); however, there were no significant interaction effect. There

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was also no interaction among fines, metals, and day (p = 0.225).

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Although there were effects of metal contamination on community

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composition throughout the experiment, differences between treatments with

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(treatments C and F) and without (treatments A, B, D, and E) metal-contaminated fine

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sediment were greatest on day 30 (Figure 3). Treatments with metal-fines were only

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significantly different from treatments with no-fines on day 5 (p < 0.01); however, on day

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30 all fine-sediment treatments were significantly different from one another (p < 0.05).

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Greater separation between communities on reference-coarse (treatments A-C) and

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metal-coarse (treatments D-F) trays were observed early in the experiment.

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Additionally, based on NMDS plots, benthic invertebrate abundances showed greater

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differences between reference-coarse trays over time, whereas trays with metal-coarse

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sediment became more similar (Figure 3).

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Mesocosm Experiment: The goal of the mesocosm experiment was to

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determine if benthic invertebrates from reference communities could colonize reference

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substrate located downstream of contaminated substrate. All community metrics were

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significantly affected by tray position (source vs. treatment vs. sink trays; Table S5).

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The results of multivariate analysis showed that community composition was

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significantly affected by metal contamination, fine sediment and tray position. There was


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also a significant interaction of metals and tray position (p < 0.05; Table 2), with fewer

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taxa colonizing the metal-contaminated trays.

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Differences in colonization between treatments and tray position were

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visualized in NMDS plots (Figure 4). In each treatment, communities from the source

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population were significantly different from all downstream trays. In the streams with

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no-fine sediment treatments (treatments A and D; Figure 1a), we observed significant

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differences (p < 0.05) in community composition between all trays, which were largely

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due to greater abundance of chironomids in the sink trays (Table S6). Trays with metal-

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coarse treatments (treatments D, E, and F; Figure 1a) showed greater separation

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between all trays, particularly between the treatment trays and sinks trays (Figure 4).

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The difference between the source and downstream trays in streams with reference and

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metal fine-sediment treatments were largely due to several mayflies, stoneflies and

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caddisflies (e.g., Capnia sp., Rhithrogena sp., Rhyacophila sp., Zapada sp., and

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Taenionema sp.) that failed to colonize downstream trays (Table S6).

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We analyzed four groups of functional traits (drift frequency, swimming ability,

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habitat preference, feeding guild) that could provide insight into the role of taxa mobility

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and ecological niche in downstream colonization of reference-coarse (treatment A) and

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metal-coarse + fines (treatment F) treatments. Species that were either rare or common

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in the drift (e.g., Drunella sp., Micrasema sp., Rhyacophila sp. and Lepidostoma sp.)

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generally remained on the source trays but decreased significantly in downstream

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treatment and sink trays (Figure 5). In contrast, species defined as abundant in the drift

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(e.g., Baetis sp. and Chironomidae) increased significantly in sink trays and were the

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only organisms reduced on metal-contaminated substrate. Although we observed



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significant differences between substrate treatments based on swimming ability, habitat

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preference and feeding guild, larger differences were associated with tray position, as

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organisms consistently avoided trays with contaminated substrate (Figure S3).

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Significant interactions between metal treatment and tray position resulted from greater

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separation among trays in streams with metal-contaminated substrate (treatment F)

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compared to reference substrate (treatment A; Table S7).

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DISCUSSION

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The most important finding of our research was that macroinvertebrate

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communities responded quite differently to the effects of metal contamination and

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sediment deposition in both the field and in stream mesocosms. Although previous

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research has investigated the adverse effects of metal contamination on benthic

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communities,1,33,38 few studies have examined the combined effects of metals and fine

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sediment deposition. Because these stressors often co-occur,28–30 understanding their

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combined and interactive effects is critical for predicting responses to restoration of

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mine-polluted watersheds.

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Construction of a water treatment plant on the NFCC is expected to result in a

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rapid decrease in metals discharged to the system. Despite these predicted

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improvements in water quality, our results suggest metal-contaminated sediments, both

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coarse and fine, will likely impede benthic invertebrate colonization downstream. In

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particular, metal contamination had the greatest impact on early colonizing taxa, such

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as Baetis sp. and Chironomidae (Orthocladiinae and Diamesinae). These taxa are

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dominant at NFCC and very common in the drift49, which may explain why they rapidly

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colonized trays in our field experiment. Both groups were also sensitive to metals in 18 ACS Paragon Plus Environment

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coarse and fine sediments, especially early in the study. This trend was also observed

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in our mesocosm experiment where baetids and chironomids avoided metal-

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contaminated coarse and fine treatments.

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The primary hypothesis that motivated our mesocosm study was that patches of

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contaminated substrate may act as barriers to downstream colonization. Although this

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idea is not new, to our knowledge the application of patch dynamics within the context

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of chemical stressors in lotic ecosystems has not been investigated experimentally. In

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our study, this hypothesis was supported for caddisflies and some stoneflies, but

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generally communities on source and sink trays were very similar. However, inability of

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some less mobile taxa to colonize downstream of contaminated habitats, as well as

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lower diversity and richness downstream, supports the hypothesis that chemical and

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physical stressors will create habitat patches following improvements in water quality at

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NFCC. Although most organisms avoided contaminated substrates in our mesocosm

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study, some taxa were abundant on the downstream sink trays. This was especially true

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for highly mobile organisms that were abundant in the drift. Interestingly, these same

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organisms were also significantly reduced in mesocosms containing metal-

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contaminated substrate, suggesting greater mortality of these highly mobile species.

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The ability of some invertebrates (e.g., Baetis sp.) to rapidly colonize clean habitat

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creates significant patchiness in their abundance and distribution. Because of the

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increased patchiness of benthic invertebrates at contaminated sites,7 there needs to be

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careful consideration of sampling methods and necessary sample sizes to detect

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effects.51



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One of the major criticisms of traditional laboratory toxicity tests is the lack of

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ecological realism and the inability to account for processes such as insect emergence,

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predator-prey interactions, or behavioral avoidance. Using a combination of field

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studies, community-level experiments, and laboratory toxicity tests, we may be able to

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improve predictions of community responses to contaminants and other anthropogenic

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stressors. This study suggests that behavioral avoidance and the inability of some taxa

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to colonize contaminated patches of substrate complicate the ability to predict

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responses to, and recovery from mining discharges.

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One underlying question is whether the outcome of laboratory toxicity and single-

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contaminant experiments can be used to predict responses in the field. Several studies

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indicate that Chironomidae are generally more tolerant to metals than other taxa;33,52

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however, in the current study chironomids (primarily Orthocladiinae) generally avoided

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metal-contaminated substrate in mesocosm and field experiments. This may indicate

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that some chironomids are more sensitive to metals than previously thought, since the

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ecological consequences of avoidance and mortality are similar.35 In contrast to the

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patterns for metal contamination, some of the variation in abundance of chironomids

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was explained by the amount of fine sediment in trays, which provided important habitat

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for these burrowing organisms. Field and mesocosm approaches play a critical role in

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addressing questions about the recovery of taxa after exposure to multiple

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anthropogenic disturbances. These experiments also demonstrate the importance of

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accounting for colonization ability, behavioral avoidance and patch dynamics when

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assessing impacts of mining on streams. Although our mesocosms cannot be

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completely scaled to the field, it is expected that patches of suitable habitat will be


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available for colonization downstream after restoration. While some invertebrates

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experience direct mortality due to metal exposure, avoidance of patches of metal-

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contaminated substrate may be a more important factor determining community

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composition following stream restoration.

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Previous investigators have measured effects of contaminated substrate on

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colonization dynamics and recovery potential of benthic macroinvertebrates.22,38 For

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example, recovery potential based on tolerance to aqueous metals, avoidance of metal-

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contaminated coarse substrate and natural drift propensity of benthic invertebrates have

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been previously estimated.38 Although natural drift propensity may determine the

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movement of macroinvertebrates to downstream habitat patches, the present study

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suggests that recovery of some macroinvertebrates is also influenced by avoidance of

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fine sediments. Avoidance of fine sediment is likely due to the loss of habitat and

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interstitial spaces for macroinvertebrates.4,5,7 Since many taxa at NFCC are adapted to

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cobble and gravel bed habitats typical of high gradient streams, patches of fine

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sediment deposition may act as habitat filters for macroinvertebrates.53 Because initial

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recovery of mining-disturbed streams may largely depend on avoidance of

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contaminated patches, these findings demonstrate the need to develop a better

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understanding of species traits in response to mining disturbance and the importance of

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accounting for multiple stressors when assessing recovery potential of disturbed

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watersheds.

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In conclusion, our field and mesocosm experiments provided insights into

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recovery potential that could not be obtained using traditional laboratory or field

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bioassessment approaches. Although our experiments were relatively short-term, we



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determined how several dominant taxa were affected by mining disturbance and

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predicted how benthic communities would likely respond during the early and late

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stages of recovery following stream restoration. Our findings also suggest that the high

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variability and rapid recolonization of aquatic insects downstream from sources of metal

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contamination and fine sediment may increase population patchiness. We also

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identified important interspecific differences in the response to metals and sediment

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deposition. In the present study Baetis sp. avoided metal-contaminated coarse

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substrate, whereas chironomids were relatively sensitive to metal-contaminated fine

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sediment. These inconsistencies between traditional laboratory studies and responses

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in field and mesocosm experiments demonstrate the need to develop more creative

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approaches to quantify effects of multiple stressors. By accounting for ecological

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factors such as patch dynamics, biological traits and colonization we could improve our

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ability to predict success of stream restorations programs and reduce the likelihood of

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over- or underestimating effects of contaminants.

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ACKNOWLEDGEMENTS

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We thank Hannah Riedl, Brian Wolff, Graham Buggs, and Kalli Jimmie for their

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assistance in the field and laboratory. This material is based upon work supported by

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the National Science Foundation Graduate Research Fellowship (Grant No. 1321845)

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provided to B.D. Any opinion, findings, and conclusions or recommendations expressed

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in this material are those of the authors and do not necessarily reflect the views of the


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National Science Foundation. Support was also provided to J.R., W.C., and J.W. by the

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National Institute of Environmental Health Sciences (1R01ES020917-01)

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ASSOCIATED CONTENT

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Supporting Information

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Supporting information includes figures of the study site (Figure S1) and composition of

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trait groups in mesocosm experiment (Figure S2), and tables showing results of metal

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concentrations (Table S1), sediment and organic matter concentrations (Table S2) and

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correlations to community composition (Table S3), ANOVA outputs for field (Table S4)

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and mesocosm (Table S5) experiments, pairwise-comparisons and SIMPER output for

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the mesocosm experiment (Table S6), and pairwise comparisons of communities by

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tray position (Table S7).

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AUTHOR INFORMATION

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Corresponding Author

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*Brittanie Dabney

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Email: [email protected] ORCID: 0000-0002-7100-7600



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Table 1: Results of PERMANOVA tests showing effects of metals, fine sediment and sampling

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day on community composition in the field experiment. p-values

Influence of Metal Contamination and Sediment Deposition on Benthic

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