Influence of metal contamination and sediment deposition on benthic

Mountain streams where most species are adapted to cobble and gravel-bed habitats. 73 that provide enough ...... Figure legends. Figure 1: (a) Schemat...
0 downloads 0 Views 1MB Size
Subscriber access provided by READING UNIV

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

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 39

Environmental Science & Technology

1

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

2

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

3

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

4

Ranville2

5

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

6

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

7

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

8

Corresponding Author: Brittanie L. Dabney

9

Department of Environmental Toxicology,

10

Texas Tech University, Lubbock, TX 79409.

11

Email: [email protected]

12

ORCID: 0000-0002-7100-7600

i ACS Paragon Plus Environment

Environmental Science & Technology

13

TOC/Abstract Graphic

14

ii ACS Paragon Plus Environment

Page 2 of 39

Page 3 of 39

15 16

Environmental Science & Technology

ABSTRACT Assessing benthic invertebrate community responses to multiple stressors is

17

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

18

mesocosm and field experiments were integrated to predict how benthic

19

macroinvertebrate communities would recover following the removal of acid mine

20

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

21

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

22

upstream reference site where colonization by benthic macroinvertebrates was

23

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

24

the hypothesis that patches of metal-contaminated substrate impede recolonization

25

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

26

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

27

Community assemblages in treatments with metal-contaminated fine substrate were

28

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

29

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

30

community structure between streams with metal-contaminated sediments and

31

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

32

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

33

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

34

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

iii ACS Paragon Plus Environment

Environmental Science & Technology

35 36

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

37

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

38

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

39

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

40

streambed homogenization, contaminant-loading and alterations of ecosystem

41

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

42

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

43

physical stress by abrasion and disruption of benthic invertebrate community

44

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

45

activities continues to degrade aquatic ecosystems, restoration managers require

46

information on macroinvertebrate community responses if they hope to improve the

47

likelihood of success in restoring mined watersheds.

48

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

49

macroinvertebrates has mostly focused on single-species laboratory tests and

50

observational studies. Observational studies show low benthic invertebrate

51

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

52

responses to fine sediment accumulation have been reported from field experimental

53

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

54

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

55

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

56

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

57

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

4 ACS Paragon Plus Environment

Page 4 of 39

Page 5 of 39

Environmental Science & Technology

58

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

59

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

60

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

61

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

62

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

63

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

64

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

65

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

66

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

67

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

68

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

69

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

70

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

71

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

72

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

73

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

74

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

75

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

76

distributions in streams.4,32

77

The ability of macroinvertebrates to recolonize previously disturbed areas has

78

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

79

are lacking. Understanding how macroinvertebrates respond following a disturbance is

80

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

5 ACS Paragon Plus Environment

Environmental Science & Technology

81

Additionally, behavioral avoidance of contaminated sediments, which has been

82

understudied in macroinvertebrate communities, can provide a more environmentally

83

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

84

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

85

sediment deposition on benthic invertebrate communities. We performed a field

86

experiment with the objective of predicting responses of benthic invertebrate

87

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

88

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

89

Environmental stressors may increase the patchiness of benthic invertebrate

90

populations in lotic environments and influence populations colonizing downstream

91

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

92

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

93

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

94

hypothesis that contaminated habitats influence downstream colonization, and the

95

likelihood of benthic invertebrate movement beyond patches of contaminated sediment.

96

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

97

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

98

responses influenced downstream colonization in our mesocosm experiment. These

99

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

100

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

101

the effects of multiple stressors on the distribution and recruitment of

102

macroinvertebrates in restored streams.

6 ACS Paragon Plus Environment

Page 6 of 39

Page 7 of 39

Environmental Science & Technology

103

MATERIALS AND METHODS

104

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

105

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

106

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

107

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

108

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

109

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

110

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

111

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

112

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

113

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

114

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

115

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

116

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

117

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

118

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

119

from mining and other anthropogenic activities.

120 121

Field Experiment: The colonization experiment was performed upstream of the

122

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

123

Physicochemical characteristics of the reference site were monitored throughout the

124

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

125

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

7 ACS Paragon Plus Environment

Environmental Science & Technology

126

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

127

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

128

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

129

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

130

Because recolonization of the downstream reaches will occur predominantly from

131

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

132

stressors.

133

Metal contaminated sediments were collected in NFCC near the source of

134

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

135

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

136

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

137

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

138

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

139

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

140

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

141

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


255

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

256

tests.48

257

Mobility and ecology traits were assessed based on a comprehensive trait

258

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

259

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

260

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

261

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

262

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

13 ACS Paragon Plus Environment

Environmental Science & Technology

263

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

264

macroinvertebrate communities were examined. For trait comparisons, only treatments

265

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

266

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

267

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

268

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

269

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

270 271 272

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

273

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

274

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

275

trays were not significantly different throughout the experiment and concentrations in

276

the metal treatments approximated values measured at our metal-contaminated

277

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

278

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

279

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

280

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

281

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

282

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

283

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

284

matter was the most important variable influencing macroinvertebrate trends in all

285

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

14 ACS Paragon Plus Environment

Page 14 of 39

Page 15 of 39

286

Environmental Science & Technology

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

287

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

288

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

289

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

290

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

291

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

292

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

293

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

294

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

295

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

296

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

297

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

298

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

299

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

300

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

301

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

302

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

303

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

304

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

305

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

306

specific responses to metal-contaminated fines were variable throughout the

307

experiment.

15 ACS Paragon Plus Environment

Environmental Science & Technology

308

Results of multivariate analysis showed that community assemblages

309

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

310

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

311

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

312

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

313

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

314

Although there were effects of metal contamination on community

315

composition throughout the experiment, differences between treatments with

316

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

317

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

318

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

319

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

320

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

321

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

322

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

323

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

324

sediment became more similar (Figure 3).

325

Mesocosm Experiment: The goal of the mesocosm experiment was to

326

determine if benthic invertebrates from reference communities could colonize reference

327

substrate located downstream of contaminated substrate. All community metrics were

328

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

329

The results of multivariate analysis showed that community composition was

330

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

16 ACS Paragon Plus Environment

Page 16 of 39

Page 17 of 39

Environmental Science & Technology

331

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

332

taxa colonizing the metal-contaminated trays.

333

Differences in colonization between treatments and tray position were

334

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

335

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

336

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

337

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

338

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

339

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

340

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

341

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

342

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

343

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

344

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

345

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

346

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

347

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

348

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

349

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

350

generally remained on the source trays but decreased significantly in downstream

351

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

352

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

353

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

17 ACS Paragon Plus Environment

Environmental Science & Technology

354

significant differences between substrate treatments based on swimming ability, habitat

355

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

356

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

357

Significant interactions between metal treatment and tray position resulted from greater

358

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

359

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

360

DISCUSSION

361 362

The most important finding of our research was that macroinvertebrate

363

communities responded quite differently to the effects of metal contamination and

364

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

365

research has investigated the adverse effects of metal contamination on benthic

366

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

367

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

368

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

369

mine-polluted watersheds.

370

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

371

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

372

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

373

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

374

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

375

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

376

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

377

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

Page 18 of 39

Page 19 of 39

Environmental Science & Technology

378

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

379

in our mesocosm experiment where baetids and chironomids avoided metal-

380

contaminated coarse and fine treatments.

381

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

382

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

383

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

384

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

385

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

386

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

387

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

388

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

389

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

390

NFCC. Although most organisms avoided contaminated substrates in our mesocosm

391

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

392

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

393

organisms were also significantly reduced in mesocosms containing metal-

394

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

395

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

396

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

397

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

398

careful consideration of sampling methods and necessary sample sizes to detect

399

effects.51

19 ACS Paragon Plus Environment

Environmental Science & Technology

400

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

401

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

402

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

403

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

404

improve predictions of community responses to contaminants and other anthropogenic

405

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

406

to colonize contaminated patches of substrate complicate the ability to predict

407

responses to, and recovery from mining discharges.

408

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

409

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

410

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

411

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

412

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

413

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

414

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

415

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

416

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

417

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

418

addressing questions about the recovery of taxa after exposure to multiple

419

anthropogenic disturbances. These experiments also demonstrate the importance of

420

accounting for colonization ability, behavioral avoidance and patch dynamics when

421

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

422

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

20 ACS Paragon Plus Environment

Page 20 of 39

Page 21 of 39

Environmental Science & Technology

423

available for colonization downstream after restoration. While some invertebrates

424

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

425

contaminated substrate may be a more important factor determining community

426

composition following stream restoration.

427

Previous investigators have measured effects of contaminated substrate on

428

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

429

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

430

contaminated coarse substrate and natural drift propensity of benthic invertebrates have

431

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

432

movement of macroinvertebrates to downstream habitat patches, the present study

433

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

434

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

435

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

436

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

437

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

438

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

439

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

440

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

441

accounting for multiple stressors when assessing recovery potential of disturbed

442

watersheds.

443

In conclusion, our field and mesocosm experiments provided insights into

444

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

445

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

21 ACS Paragon Plus Environment

Environmental Science & Technology

446

determined how several dominant taxa were affected by mining disturbance and

447

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

448

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

449

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

450

contamination and fine sediment may increase population patchiness. We also

451

identified important interspecific differences in the response to metals and sediment

452

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

453

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

454

sediment. These inconsistencies between traditional laboratory studies and responses

455

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

456

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

457

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

458

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

459

over- or underestimating effects of contaminants.

460 461 462 463

ACKNOWLEDGEMENTS

464

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

465

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

466

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

467

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

468

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

22 ACS Paragon Plus Environment

Page 22 of 39

Page 23 of 39

Environmental Science & Technology

469

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

470

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

471

ASSOCIATED CONTENT

472 473

Supporting Information

474

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

475

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

476

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

477

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

478

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

479

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

480

tray position (Table S7).

481

AUTHOR INFORMATION

482

Corresponding Author

483

*Brittanie Dabney

484

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

23 ACS Paragon Plus Environment

Environmental Science & Technology

REFERENCES

485 486

(1)

Clements, W. H.; Carlisle, D. M.; Lazorchak, J. M.; Johnson, P. C. Heavy metals

487

structure benthic communities in Colorado mountain streams. Ecol. Appl. 2000,

488

10 (2), 626–638.

489

(2)

Hornberger, M. I.; Luoma, S. N.; Johnson, M. L.; Holyoak, M. Influence of

490

remediation in a mine-impacted river: metal trends over large spatial and temporal

491

scales. Ecol. Appl. 2009, 19 (6), 1522–1535.

492

(3)

Daniel, W. M.; Infante, D. M.; Hughes, R. M.; Tsang, Y. P.; Esselman, P. C.;

493

Wieferich, D.; Herreman, K.; Cooper, A. R.; Wang, L.; Taylor, W. W.

494

Characterizing coal and mineral mines as a regional source of stress to stream

495

fish assemblages. Ecol. Indic. 2015, 50, 50–61.

496

(4)

environment. Environ. Manage. 1997, 21 (2), 203–217.

497 498

(5)

Waters, T. F. Sediment in streams: sources, biological effects, and control; American Fisheries Society Monograph 7: Bethes, Maryland, USA, 1995.

499 500

Wood, P. J.; Armitage, P. D. Biological effects of fine sediment in the lotic

(6)

Smolders, A. J. P.; Lock, R. A. C.; Van der Velde, G.; Medina Hoyos, R. I.;

501

Roelofs, J. G. M. Effects of mining activities on heavy metal concentrations in

502

water, sediment, and macroinvertebrates in different reaches of the Pilcomayo

503

River, South America. Arch. Environ. Contam. Toxicol. 2003, 44 (3), 314–323.

504

(7)

multiple stressors. Environ. Toxicol. Chem. 2010, 29 (12), 2625–2643.

505 506 507

Burton, G. A.; Johnston, E. L. Assessing contaminated sediments in the context of

(8)

Chutter, F. M. The effect of sand and silt on the invertebrate fauna of streams and rivers. Hydrobiologia 1969, 34 (1), 57–76.

24 ACS Paragon Plus Environment

Page 24 of 39

Page 25 of 39

508 509 510

Environmental Science & Technology

(9)

Erman, D. C.; Erman, N. A. The response of stream macroinvertebrates to substrate size and heterogeneity. Hydrobiologia 1984, 108 (1), 75–82.

(10) Rumisha, C.; Elskens, M.; Leermakers, M.; Kochzius, M. Trace metal pollution

511

and its influence on the community structure of soft bottom molluscs in intertidal

512

areas of the Dar es Salaam coast, Tanzania. Mar. Pollut. Bull. 2012, 64 (3), 521–

513

531.

514

(11) Jones, J. I.; Murphy, J. F.; Collins, A. L.; Sear, D. A.; Naden, P. S.; Armitage, P.

515

D. The impact of fine sediment on macro-invertebrates. River Res. Appl. 2012, 28

516

(8), 1055–1071.

517

(12) Wright, I. A.; Ryan, M. M. Impact of mining and industrial pollution on stream

518

macroinvertebrates: importance of taxonomic resolution, water geochemistry and

519

EPT indices for impact detection. Hydrobiologia 2016, 772 (1), 103–115.

520

(13) Clements, W. H. Small-scale experiments support causal relationships between

521

metal contamination and macroinvertebrate community responses. Ecol. Appl.

522

2004, 14 (3), 954–967.

523

(14) Larsen, S.; Pace, G.; Ormerod, S. J. Experimental effects of sediment deposition

524

on the structure and function of macroinvertebrate assemblages in temperate

525

streams. River Res. Appl. 2011, 27 (2), 257–267.

526

(15) Mathers, K. L.; Wood, P. J. Fine sediment deposition and interstitial flow effects

527

on macroinvertebrate community composition within riffle heads and tails.

528

Hydrobiologia 2016, 776 (1), 147–160.

529 530

(16) Dias, V.; Vasseur, C.; Bonzom, J. M. Exposure of Chironomus riparius larvae to uranium: Effects on survival, development time, growth, and mouthpart

25 ACS Paragon Plus Environment

Environmental Science & Technology

531 532

deformities. Chemosphere 2008, 71 (3), 574–581. (17) Gale, S. A.; King, C. K.; Hyne, R. V. Chronic sublethal sediment toxicity testing

533

using the estuarine amphipod , Melita plumulosa (Zeidler): Evaluation using

534

metal-spiked and field-contaminated sediments. Environ. Toxicol. Chem. 2006, 25

535

(7), 1887–1898.

536

(18) Cain, D. J.; Carter, J. L.; Fend, S. V.; Luoma, S. N.; Alpers, C. N.; Taylor, H. E.

537

Metal exposure in a benthic macroinvertebrate, Hydropsyche californica, related

538

to mine drainage in the Sacramento River. Can. J. Fish. Aquat. Sci. 2000, 57 (2),

539

380–390.

540

(19) Williams, N.; Rizzo, A.; Arribére, M. A.; Suárez, D. A.; Guevara, S. R. Silver

541

bioaccumulation in chironomid larvae as a potential source for upper trophic

542

levels: a study case from northern Patagonia. Environ. Sci. Pollut. Res. 2017, 1–

543

12.

544

(20) Goodyear, K. L.; McNeill, S. Bioaccumulation of heavy metals by aquatic macro-

545

invertebrates of different feeding guilds: a review. Sci. Total Environ. 1999, 229

546

(1), 1–19.

547

(21) Ward, D. J.; Simpson, S. L.; Jolley, D. F. Slow avoidance response to

548

contaminated sediments elicits sublethal toxicity to benthic invertebrates. Environ.

549

Sci. Technol. 2013, 47 (11), 5947–5953.

550

(22) Courtney, L. A.; Clements, W. H. Assessing the influence of water and substratum

551

quality on benthic macroinvertebrate communities in a metal-polluted stream: An

552

experimental approach. Freshw. Biol. 2002, 47, 1776–1778.

553

(23) Camusso, M.; Polesello, S.; Valsecchi, S.; Vignati, D. A. L. Importance of dietary

26 ACS Paragon Plus Environment

Page 26 of 39

Page 27 of 39

Environmental Science & Technology

554

uptake of trace elements in the benthic deposit-feeding Lumbriculus variegatus.

555

Trends Anal. Chem. 2012, 36, 103–112.

556

(24) Rainbow, P. S.; Smith, B. D.; Luoma, S. N. Biodynamic modelling and the

557

prediction of Ag, Cd and Zn accumulation from solution and sediment by the

558

polychaete Nereis diversicolor. Mar. Ecol. Prog. Ser. 2009, 390, 145–155.

559

(25) Lefcort, H.; Abbott, D. P.; Cleary, D. A.; Howell, E.; Keller, N. C.; Smith, M. M.

560

Aquatic snails from mining sites have evolved to detect and avoid heavy metals.

561

Arch. Environ. Contam. Toxicol. 2004, 46 (4), 478–484.

562

(26) Townsend, C. R.; Uhlmann, S. S.; Matthaei, C. D. Individual and combined

563

responses of stream ecosystems to multiple stressors. J. Appl. Ecol. 2008, 45 (6),

564

1810–1819.

565

(27) Fausch, K. D.; Baxter, C. V.; Murakami, M. Multiple stressors in north temperate

566

streams: Lessons from linked forest-stream ecosystems in northern Japan.

567

Freshw. Biol. 2010, 55 (SUPPL. 1), 120–134.

568

(28) Zapico, I.; Laronne, J. B.; Martín-Moreno, C.; Martín-Duque, J. F.; Ortega, A.;

569

Sánchez-Castillo, L. Baseline to evaluate off-site suspended sediment-related

570

mining effects in the Alto Tajo Natural Park, Spain. L. Degrad. Dev. 2017, 28 (1),

571

232–242.

572

(29) Chalov, S. R. Effects of placer mining on suspended sediment budget: case study

573

of north of Russia’s Kamchatka Peninsula. Hydrol. Sci. J. 2014, 59 (5), 1081–

574

1094.

575

(30) Jarsjö, J.; Chalov, S. R.; Pietroń, J.; Alekseenko, A. V.; Thorslund, J. Patterns of

576

soil contamination, erosion and river loading of metals in a gold mining region of

27 ACS Paragon Plus Environment

Environmental Science & Technology

577

northern Mongolia. Reg. Environ. Chang. 2017, 17 (7), 1991–2005.

578

(31) Coulthard, T. J.; Macklin, M. G. Modeling long-term contamination in river

579 580

systems from historical metal mining. Geology 2003, 31 (5), 451–454. (32) Richards, C.; Bacon, K. L. Influence of fine sediment on macroinvertebrate

581

colonization of surface and hyporheic stream substrates. Gt. Basin Nat. 1994, 54

582

(2), 106–113.

583

(33) Clements, W. H.; Vieira, N. K.; Church, S. E. Quantifying restoration success and

584

recovery in a metal-polluted stream: a 17-year assessment of physicochemical

585

and biological responses. J. Appl. Ecol. 2010, 47 (4), 899–910.

586

(34) Gergs, A.; Classen, S.; Strauss, T.; Ottermanns, R.; Brock, T. C. M.; Ratte, H. T.;

587

Hommen, U.; Preuss, T. G. Ecological recovery potential of freshwater organisms:

588

consequences for environmental risk assessment of chemicals. In Reviews of

589

Environmental Contamination and Toxicology; Springer, Cham, 2016; Vol. 236,

590

pp 259–294.

591

(35) Araújo, C. V. M.; Moreira-Santos, M.; Ribeiro, R. Active and passive spatial

592

avoidance by aquatic organisms from environmental stressors: A complementary

593

perspective and a critical review. Environ. Int. 2016, 92–93, 405–415.

594

(36) Lake, P. S. Disturbance, patchiness, and diversity in streams. J. North Am.

595

Benthol. Soc. 2000, 19 (4), 573–592.

596

(37) Kiffney, P. M.; Greene, C. M.; Hall, J.; Davies, J. Tributary streams create spatial

597

discontinuities in habitat, biological productivity, and diversity in mainstem rivers.

598

Can. J. Fish. Aquat. Sci. 2006, 63 (11), 2518–2530.

599

(38) Cadmus, P.; Clements, W. H.; Williamson, J. L.; Ranville, J. F.; Meyer, J. S.;

28 ACS Paragon Plus Environment

Page 28 of 39

Page 29 of 39

Environmental Science & Technology

600

Gutiérrez Ginés, M. J. The use of field and mesocosm experiments to quantify

601

effects of physical and chemical stressors in mining-contaminated streams.

602

Environ. Sci. Technol. 2016, 50 (14), 7825–7833.

603

(39) Butler, B. A.; Ranville, J. F.; Ross, P. E. Spatial variations in the fate and transport

604

of metals in a mining-influenced stream, North Fork Clear Creek, Colorado. Sci.

605

Total Environ. 2009, 407 (24), 6223–6234.

606

(40) Clements, W. H.; Cherry, D. S.; Cairns Jr, J. Impact of heavy metals on insect

607

communities in streams: a comparison of observational and experimental results.

608

Can. J. Fish. Aquat. Sci. 1988, 45 (11), 2017–2025.

609 610 611

(41) An Introduction to the Aquatic Insects of North America, 4th, ed.; Merritt, R. W., Cummins, K. W., Berg, M. B., Eds.; Kendall Hunt Publishing: Dubuque, IA, 2008. (42) Ward, J. V; Kondratieff, B. C.; Zuellig, R. E. An Illustrated Guide to the Mountain

612

Stream Insects of Colorado, Second.; University Press of Colorado: Boulder, CO,

613

2002.

614

(43) Murray, K. S.; Cauvet, D.; Lybeer, M.; Thomas, J. C. Particle size and chemical

615

control of heavy metals in bed sediment from the Rouge River, southeast

616

Michigan. Environ. Sci. Technol. 1999, 33 (7), 987–992.

617

(44) MacDonald, D. D.; Ingersoll, C. G.; Berger, T. A. Development and evaluation of

618

consensus-based sediment quality guidelines for freshwater ecosystems. Arch.

619

Environ. Contam. Toxicol. 2000, 39 (1), 20–31.

620 621 622

(45) Anderson, M. J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001, 26 (1), 32–46. (46) Clarke, K. R.; Green, R. H. Statistical design and analysis for a “biological effects”

29 ACS Paragon Plus Environment

Environmental Science & Technology

623 624

study. Mar. Ecol. Prog. Ser. 1988, 46, 213–226. (47) Anderson, M. J.; Gorley, R. N.; Clarke, K. R. Permanova+ for Primer: Guide to

625

Software and Statistical Method, 1st, ed.; PRIMER-E: Plymouth, 2008.

626

(48) Clarke, K. R.; Warwick, R. M. Change in marine communities. An approach to

627

statistical analysis and interpretation. Prim. Plymouth, UK 2001, 1–176.

628

(49) Poff, N. L.; Olden, J. D.; Vieira, N. K.; Finn, D. S.; Simmons, M. P.; Kondratieff, B.

629

C. Functional trait niches of North American lotic insects: traits-based ecological

630

applications in light of phylogenetic relationships. J. North Am. Benthol. Soc.

631

2006, 25 (4), 730–755.

632

(50) Williamson, J. L. Development and application of field methods for determination

633

of the extent of acid mine drainage contamination, and geochemical

634

characteristics of stream sediment recovery. Ph.D. Dissertation, Colorado School

635

of Mines, Golden, CO, 2016.

636

(51) Carter, J. L.; Resh, V. H. After site selection and before data analysis: sampling,

637

sorting, and laboratory procedures used in stream benthic macroinvertebrate

638

monitoring programs by USA state agencies. J. North Am. Benthol. Soc. 2001, 20

639

(4), 658–682.

640

(52) Iwasaki, Y.; Kagaya, T.; Miyamoto, K. I.; Matsuda, H. Responses of riverine

641

macroinvertebrates to zinc in natural streams: Implications for the Japanese water

642

quality standard. Water. Air. Soil Pollut. 2012, 223 (1), 145–158.

643

(53) Poff, N. L. Landscape filters and species traits: towards mechanistic

644

understanding and prediction in stream ecology. J. north Am. Benthol. Soc. 1997,

645

16 (2), 391–409.

30 ACS Paragon Plus Environment

Page 30 of 39

Page 31 of 39

Environmental Science & Technology

646 647

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

648

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