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