Transcript The accuracy and protectiveness of Biotic Ligand Model (BLM) toxicity

The accuracy and protectiveness of
Biotic Ligand Model (BLM) toxicity
predictions with copper
Christopher A. Mebane
U.S. Geological Survey, Boise, Idaho, USA
Workshop on Biotic Ligand Model Principles and
Applications
Wilfrid Laurier University, Waterloo, Ontario,
Canada
May 12-14, 2008
U.S. Department of the Interior
U.S. Geological Survey
All analyses and data summaries shown in this talk are provisional
and subject to revision
In the States, It’s not just a model, it’s the law...
At least, national criteria issued pursuant to the law.
March
, # 2
BLM promoted to provide less stringent effluent limits
“Using the new [BLM-based copper] criteria effectively”
“It is expected that the BLM-based criteria will be less stringent
in low hardness waters, but possibly more stringent in harder
waters. Therefore, wastewater treatment plants discharging into
waters with low hardness, especially with high dissolved
organic carbon, should consider performing a BLM and
proposing alternative copper effluent limits as appropriate.”
http://www.cdm.com/knowledge_center/monthly_viewpoint/
epa_copper_criteria.htm (viewed April 29, 2008)
Yukon
BLM- and hardness based chronic copper
River at Eagle, Alaska
criterion, Yukon River at Eagle, AK
BLM-CCC
16
70
Hardness-based
CCC (µg/L)
Cu CWQG (1987)
14
DOC
10
40
8
30
6
20
4
Date
Jul-2005
Apr-2005
Jan-2005
Oct-2004
Jul-2004
Apr-2004
Jan-2004
Oct-2003
Jul-2003
Apr-2003
Jan-2003
Oct-2002
Jul-2002
Apr-2002
Jan-2002
Oct-2001
0
Jul-2001
0
Apr-2001
2
Jan-2001
10
USGS Photo
DOC (mg/L)
12
50
Oct-2000
Copper (µg/l)
60
2,000
2
0
0
Jul-2004
Apr-2004
Jan-2004
20,000
Yukon River
DOC
14,000
12,000
10
10,000
8
8,000
6
6,000
4,000
4
Date
USGS Photo
DOC (mg/L)
Flow
Oct-2003
Jul-2003
Apr-2003
18,000
Jan-2003
Oct-2002
Jul-2002
Apr-2002
Jan-2002
Oct-2001
Jul-2001
Apr-2001
Jan-2001
Oct-2000
Flow (m 3/s)
criterion, Yukon River at Eagle, AK
16
14
16,000
12
BLM-based acute copper criterion, Columbia River
Columbia River between
Northport,
WA and Trail, BC
at Northport,
WA, 1995-2000
12
Ambient Copper
BLM-CCC
10
Hardness-based CCC
CWQG (1987)
6
4
2
Aug-2000
May-2000
Feb-2000
Nov-1999
Aug-1999
May-1999
Feb-1999
Nov-1998
Aug-1998
May-1998
Feb-1998
Nov-1997
Aug-1997
May-1997
Feb-1997
Nov-1996
Aug-1996
May-1996
Feb-1996
0
Nov-1995
Copper (µg/l)
8
Date
Uncredited photo, www.city-data.com
Northwestern soft water salmon stream, Big Soos Creek, WA
BLM- and hardness based chronic copper
criterion, Big Soos Creek, Auburn, WA
30
BLM-CCC
Hardness-based CCC (EPA 2002), µg/L)
25
Ontario 1994 PWQO
15
10
5
Apr-1998
Feb-1998
Dec-1997
Oct-1997
Aug-1997
Jun-1997
Apr-1997
Feb-1997
Dec-1996
Oct-1996
Aug-1996
Jun-1996
Apr-1996
Feb-1996
0
Dec-1995
Copper (µg/l)
CWQG (1987)
20
Date
Photo King County Department of Parks and Natural Resources
Extremely soft water stream
North Fork
Coeur
Enaville,
Idaho,
BLMand d’Alene
hardnessRiver
basedatchronic
copper
criterion, NF
Coeur
River
Hardness 11-23 mg/L, DOC
0.8d'Alene
to 1.1 mg/L
6
BLM-CCC
CWQG (1987)
Ontario 1994 PWQO
Copper (µg/l)
5
4
3
2
1
0
99 999 999 999 999 999 999 999 999 999 000 000
9
1
-1 y-1 n-1
-1
-1 p-1 ct -1 v-1 c-1 n-2 b-2
ul- ug
ar Apr
a
u
J
O
M
M
J
A
No De
Ja
Fe
Se
Date
USFS Photo
Snake River leaving Yellowstone National Park, Wyoming
(hardness 25-60 mg/L, pH 7 to 8.5, DOC 0.9 to 4.5 mg/L)
BLM- and hardness based chronic copper criterion, Snake River above
Jackson Lake, WY
18
16
Copper (µg/l)
14
BLM-based CCC (µg/L)
12
10
Hardness-capped CCC
(NTR, µg/L)
8
6
4
Ontario 1994 PWQO
CWQG (1987)
2
Ap
r-1
9
93
Oc
t -1
99
3
Ap
r-1
99
4
Oc
t -1
99
4
Ap
r-1
99
5
Oc
t -1
99
5
Ap
r-1
99
6
Oc
t -1
99
6
Ap
r-1
99
7
Oc
t -1
99
7
Ap
r-1
99
8
Oc
t -1
99
8
Ap
r-1
99
9
Oc
t -1
99
9
Ap
r-2
00
0
Oc
t -2
00
0
Ap
r-2
00
1
Oc
t -2
00
1
Ap
r-2
00
2
Oc
t -2
00
2
Ap
r-2
00
3
Oc
t -2
00
3
Ap
r-2
00
4
0
Date
Copper contaminated western mountain stream, Panther Creek,
Panther
Idaho
spring
Idaho (DOC 1.1 to
4.6 mg/L,Creek,
hardness
25-50,
pH 7.5runoff
to 8.6)
5
25
BLM-CCC
Hardness-equation criteria
0
0
29
22
15
8M
-M
ar
5Ap
r
12
-A
pr
19
-A
pr
26
-A
pr
3M
ay
10
-M
ay
17
-M
ay
24
-M
ay
31
-M
ay
1
-M
ar
5
-M
ar
2
ar
10
ar
3
DOC (mg/L)
4
DOC
15
1M
Copper (µg/l)
20
1994
Data from Stratus Consulting
Copper and DOC concentrations rose together during early
snowmelt
Panther Creek, Idaho spring runoff
5
160
BLM-CCC
Ambient Cu
DOC
4
100
3
80
2
60
40
1
20
0
-M
ar
5Ap
r
12
-A
pr
19
-A
pr
26
-A
pr
3M
ay
10
-M
ay
17
-M
ay
24
-M
ay
31
-M
ay
29
-M
ar
22
-M
ar
15
ar
8M
ar
0
1M
Copper (µg/l)
120
DOC (mg/L)
140
1994
Data from Stratus Consulting
Extrapolating patterns to post-remedial conditions
25
25
5
BLM-CCC (1994)
BLM-CCC (1994)
Cu
(2005)
Cu (2005)
20
20
4
DOC (1994)
15
15
3
10
10
2
55
1
00
December
December
0
March
March
May
May
Season
July
July
DOC (mg/L)
Cu (µg/L)
Hardness-CCC
(1994)
DOC and pH data quality are important!
What’s happened in September 93?
Chronic copper criteria: Teton River at St. Anthony, ID
USGS 13055000
90
12
80
BLM-based CCC (µg/L, diss.)
10
DOC
70
8
50
6
40
30
4
20
2
10
0
Jan-93
Aug-93
Mar-94
Sep-94
Apr-95
0
Oct-95
DOC (mg/L)
Cu (µg/L)
60
DOC and pH data quality are
important!
Beware USGS DOC data prior to 1994!
Columbia River between Northport, WA and Trail, BC
12
10
95%
DOC (mg/L)
8
6
4
75%
50%
2
95%
25%
5%
5%
0
Pre-1994
1994 and later
75%
50%
25%
Colorado River downstream of Glen Canyon Dam, Arizona
12
10
DOC (mg/L)
8
6
4
2
0
A
B
Neuse River, North Carolina coastal plain
20
95%
18
16
DOC (mg/L)
14
12
75%
10
95%
50%
8
25%
75%
50%
6
25%
5%
4
5%
2
0
Pre-1994
1994 and later
Predicted Cu LC50s (µg/L)
1,000
y = 0.80x + 40
r2 = 0.88
100
10
10
100
Measured Cu LC50s (µg/L)
Data originally from Erickson 1996
1,000
1,000
Assuming DOC as 1.1
mg/L, HydroQual’s 2003
LA50 of 7.32
(DOC not measured)
Predicted Cu
100
LC50s (µg/L)
10
10
100
1,000
Measured Cu LC50s (µg/L)
1,000
Assuming DOC as 1.35 mg/L,
EPA’s 2003 LA50 of 3.56
Predicted Cu
100
LC50s (µg/L)
10
10
100
Measured Cu LC50s (µg/L)
1,000
1,000
100
Predicted Cu
LC50s (µg/L)
10
Welsh et al. (1993)
Welsh et al. (1996)
1
1
10
100
1,000
Measured Cu LC50s (µg/L)
LA50 7.32, no Mg, April 2003
DOC 100% reactive as 90% FA, 10% HA
Photo courtesy of Paul Welch
Fathead minnows in low alkalinity Precambrian Shield Lakes (Data from
Welsh et al., 1993).
DOC 100% Cu-reactive
LA50 5.48, includes Mg,
(6-10-2007)
(default)
Predicted Cu LC50s (µg/L)
1,000
100
10
Welsh et al. (1993)
Welsh et al. (1996)
1
Predicted Cu LC50s (µg/L)
1
10
100
1,000
DOC 50% Cu-reactive
Measured Cu LC50s (µg/L)
1,000
LA50 6.313, no Mg
(Recalculated from EPA
Welsh et al. (1993,1996) using HydroQual's 2007 default LA50of 5.48 includes Mg,assuming that 100% DOC is Cu2003)
reactive
100
10
Welsh et al. (1993)
Welsh et al. (1996)
1
1
10
100
Measured Cu LC50s (µg/L)
1,000
Fathead minnows in low
alkalinity South Carolina
piedmont streams
(VanGenderen et al., 2005).
Model LA50: 7.32 nmol Cu/g gill
Modified LA50: 0.2 nmol Cu/g gill
(data from VanGenderen
et al., 2005).
Predicted 96-hr Cu LC50s (µg/L)
Using EPA’s 2003 updated
dataset and assuming
50% of DOC is Cureactive
1,000
100
10
y = 0.86x + 38
r2 = 0.79
1
1
10
100
Measured 48-hr Cu LC50s (µg/L)
(top) DOC 50 % Cu-reactive,
LA50: 6.313 nmol Cu/g gill
(bottom) DOC 100% Cureactive,
LA50: 0.2 nmol Cu/g gill
VanGenderen et al. (2005) using EPA's 2003 LA50, recalculated assuming that 50% of DOC is Cu-reactive
1,000
Fatmucket, Lampsilis siliquoidea
Acute tests in waters with variable hardness and
different DOC sources
< 0.3mm
Data from Ning Wang, USGS,
Columbia, Missouri, et al., in prep.,
Photos by Doug Hardesty, USGS
Fatmucket mussel
Dissolved Cu EC50 (g/L)
400
Pond, r2=0.92
Eagle Bluffs, r2=0.96
Ditch #6, r2=0.92
Luther Marsh, r2=0.97
Humic acid, r2=0.97
300
200
100
0
0
2
4
6
DOC (mg C/L)
8
10
12
Fatmucket
A. Assume DOC is 100% reactive as 90% FA,
10% HA, (LA50 0.0605 nmol Cu/g gill)
B. Assume DOC is 50% reactive as FA
((LA50 0.1916 nmol Cu/g gill)
Pond
1000
1000
Eagle Bluffs
Predicted Cu EC50s (µg/L)
Ditch #6
B.
Luther Marsh
Humic acid
100
100
A.
Variable
hardness
Reference tests
10
y = 1.376x - 2.67
r 2 = 0.88
p <0.001
(pooling all groups)
1
10
y = 0.90x + 12.1
r 2 = 0.87
p <0.001
(pooling all groups)
1
1
10
100
Measured Cu EC50s (µg/L)
1000
1
10
100
Measured Cu EC50s (µg/L)
1000
Fatmucket mussel: hardness vs. BLM as predictor of
toxicity
y = 0.96x - 0.207
r2 = 0.9
P <0.001
(pooling all groups)
Measured EC50 (µg/L)
400
y = 0.37x +27.2
r2 = 0.05
P =0.2
(pooling all groups)
500
Pond
Eagle Bluffs
Ditch #6
Luther Marsh
Humic Acid
Variable Hardness
Reference tests
400
Measured EC50 (µg/L)
500
300
200
100
300
200
95%
prediction
bands
100
0
0
50
100
150
200
Hardness as mg/L CaCO3
250
300
0
100
200
300
BLM predicted EC50 (µg/L)
400
500
Ceriodaphnia dubia
~25 natural waters,
Mostly hardwater, (17-185 mg/L CaCO3),
DOC 0.8 to 30 mg/L
GLEC, 2006
(Tyler Linton)
Escanaba River, Michigan
photo, wikipedia.org
DOC 50% Cu-reactive
LA50 0.2378, no Mg
(Recalculated from EPA
2003)
photo, wikipedia.org
100
10
Natural waters
Mod hard reference tests
1
1
10
100
1,000
Measured Cu LC50s (µg/L)
1,000
Predicted Cu LC50s (µg/L)
DOC 100% Cu-reactive
LA50 0.0701, includes Mg,
(6-10-2007)
(default)
Predicted Cu LC50s (µg/L)
Ceriodaphnia dubia
Escanaba
River, Michigan
1,000
100
10
Natural waters
Mod hard water reference
tests
1
1
10
100
Measured Cu LC50s (µg/L)
1,000
Default
1000
Hyalella azteca
Predicted Cu LC50s (µg/L)
NOM varies (Welsh 1996)
pH,Ca vary (48hr, Collyard 2002)
pH varies (Schubauer 1993)
100
NOM series
y = 2.10x - 11.7
10
2
r = 0.9923
1
1
10
DOC as 50% AFA
100
1000
Observed Cu LC50s (µg/L)
1000
Predicted Cu LC50s (µg/L)
NOM varies (Welsh 1996)
pH,Ca vary (48hr, Collyard 2002)
pH varies (Schubauer 1993)
100
NOM series
y = 1.3137x - 7.1126
r2 = = 0.9923
10
1
1
Doug Hardesty, USGS
10
100
Observed Cu LC50s (µg/L)
1000
Welsh, Lipton, and Maest,
(Stratus Consulting)
Assume DOC is 100%
reactive as 90% FA,
10% HA
100
Predicted Cu LC50s (µg/L)
Rainbow trout flow-through
tests using natural and lab
waters, DOC <0.11 to 2.0
mg/L.
y = 1.46x + 0.65
r2 = 0.52
10
Flow through
Renewal
1
1
10
100
Predicted Cu LC50s (µg/L)
Measured Cu LC50s (µg/L)
100
y = 0.99x + 3.27
r2 = 0.58
10
Flow through
<
1
1
Josh Lipton, Stratus Consulting
Assume DOC is 50%
reactive as FA Renewal
10
Measured Cu LC50s (µg/L)
100
Chinook salmon, Sacramento River
and lab waters (default)
Chinook salmon flow-through
tests using natural and lab
waters, DOC 0.11 to 1.4 mg/L.
Welsh, Lipton, and Maest,
(Stratus Consulting)
Predicted Cu LC50s (µg/L)
100
y = 0.85x + 4.0
2
r = 0.61
10
Assume DOC is 100%
reactive as 90% FA,
10% HA
1
1
10
100
Measured Cu LC50s (µg/L)
Chinook salmon, Sacramento River and lab waters
(50% AFA)
100
Predicted Cu LC50s
(µg/L)
y = 0.62x + 3.63
2
r = 0.62
10
Assume DOC is 50% reactive
as FA
1
1
Josh Lipton, Stratus Consulting
10
Measured Cu LC50s (µg/L)
100
Rainbow trout, renewal exposures
1,000
1,000
Rainbow trout 96-h LC50
Assume DOC is
Line (perfect agreement)
100%1:1 reactive
as
2:1 Line (0.5X less toxic than
90% predicted)
FA,
1:2 Line (2X more toxic than
10% predicted)
HA
1:1 Line (perfect
agreement)
Assume
DOC
is
2:1 Line (0.5X less toxic than
50% predicted)
reactive as FA
Predicted Cu LC50s (µg/L)
Predicted Cu LC50s (µg/L)
Rainbow trout 96-h LC50
100
1:2 Line (2X more toxic than
predicted)
100
y = 0.6847x + 17.233
R2 = 0.4752
y = 0.51x + 33.927
R2 = 0.617
10
10
100
Observed Cu LC50s (µg/L)
1,000
10
10
100
1,000
Observed Cu LC50s (µg/L)
BLM Predicted vs. observed rainbow trout LC50s, in renewal tests using lab and
site waters, hardwater, DOC from <1 to 11 mg/L, 3 of 4 seasonal rounds of testing
(all data from the 1st of 4 rounds discarded for questionable DOC data).
ENSR. 1996. Development of site-specific water quality criteria for copper in the upper Clark Fork River: Phase III
WER Program testing results. ENSR Consulting and Engineering, 0480-277, Fort Collins, Colo.
from O.3 to 16 mg/L, (actual DOC mass 0.11 to 0.84 mg/L) in lab water of with
hardness of 24 mg/L CaCO3, Marr et al 1999, Panther Creek DOC analogue
Some Bad News
Predicted Cu LC50s (µg/L)
Testing DOC
“equivalents” that
matched natural DOM
for binding affinity and
complexation. DOC
equivalents ranged O.3
to 16 mg/L, (actual
DOC mass 0.11 to 0.84
mg/L) in lab water of
with hardness of 24
mg/L CaCO3,
1000
100
10
DOC cocktail equivalents
Actual DOC cocktail mass
1
1
10
100
1000
Cu LC50s
Rainbow trout 96h LC50s, uniformObserved
total hardness
with(µg/L)
varying Ca and Mg, uniform
low DOC, Welsh et al 2000
Marr et al 1999,
Panther Creek DOC
Rainbow trout 96h
LC50s, uniform total
hardness with varying
Ca and Mg, uniform
low DOC, Welsh et al
2000
Predicted Cu LC50s (µg/L)
1000
100
10
Using BLM v2.1.2 (Mg ignored)
Using v2.2.3 (Mg included)
1
1
10
100
Observed Cu LC50s (µg/L)
1000
DOC 50% reactive, as AFA
Chronic EC10s
40
Rainbow trout
35
•
•
•
•
Predicted Cu LC50s (µg/L)
Rainbow trout (30-120d
growth)
Besser et al, 2005
Hansen et al, 2002
Marr et al., 1996
Seim et al. 1984
Brook trout
30
Chinook salmon
25
20
15
10
Brook trout (2-22 months)
•
•
5
McKim et al. 1971, 1974
Sauter et al. 1976
0
0
Chinook salmon, 120d
(treated as a rainbow
trout)
•
DOC 50%
reactive,
as25AFA
15
20
10
30
35
40
100
Predicted Cu LC50s (µg/L)
Mount 1968
Welsh 1996
Besser et al. 2005
5
Observed Cu LC50s (µg/L)
Fathead Minnow (21-days
to 11 months)
•
•
•
Fathead minnow
10
1
Rainbow trout
Brook trout
Chapman 1982
Fathead minnow
Chinook salmon
0.1
0.1
1
10
Observed Cu LC50s (µg/L)
100
(McIntyre et al., ES&T, 2008)
40
BLM Predicted IC50s (µg/L)
Reductions in the olfactory
response to a natural odorant
(serine) following short-term (30
min) exposure to 20 µg/L
dissolved copper
Median olfaction IC50s assuming 100% of DOC is Cu
reactive (model default)
35
30
25
20
15
Varying DOC
10
Varying Ca
Varying alkalinity
5
0
0
10
20
30
40
Median IC50s
olfaction
IC50s (µg/L)
McIntyre olfaction
assuming
50% of DOC is Cu
reactive as FA
Photo: Carla Stehr, National
Marine Fisheries Service,
Seattle
Predicted EC50s (µg/L)
40
35
30
25
20
15
10
5
0
0
5
10
15
20
25
30
Median olfaction IC50s (µg/L)
35
40
Shayler Run, Ohio, USA
• Stream experimentally dosed
•
•
•
with copper, 1968-1972
Integrated long-term field,
streamside, and laboratory
toxicity studies
High calcium limestone
geology
DOC from natural and
sewage sources
Geckler and others, 1976.
Validity of laboratory tests
for predicting copper toxicity
in streams. EPA 600/3-76-116
Photo from Geckler and
others, 1976
BLM and field effects –Ohio Stream
90
BLM chronic criterion
80
Safe from adverse effects
(range)
Copper (µg/L)
70
Cu
(µg/L)
60
50
40
30
20
10
0
Feb-70 Aug-70
Mar-71 Sep-71 Apr-72
Oct-72 May-73
• Threshold for adverse effects from
•
•
Full life cycle streamside toxicity tests with native fish
Fish behavioral changes in stream
Convict Creek, California, USA
•
•
•
•
•
Sierra Nevada stream
experimentally dosed
with copper for 1 yr
Measured effects on
stream metabolism and
macroinvertebrate
community
Low calcium granitic
geology
Most BLM parameters
measured – except DOC
Single DOC site value of
3.7 mg/L; average DOC
in High Sierra Lakes
estimated at 1.8 mg/L.
Photo courtesy of Daniel Dawson, Sierra Nevada Aquatic Research Laboratory
BLM and field effects - Sierra Nevada stream
BLM-chronic criterion (DOC 3.7 mg/L)
Stream eco-strucure LOEC
Stream eco-function LOEC; eco-structure NOEC
BLM-chronic criterion (avg. high lakes DOC, 1.8 mg/L)
18
15
Copper
(µg/L)
12
9
6
Sources:
Leland and Carter, Freshwater
Biology,
1984, 1985, 1989
Brooks and others,
Ecosystems, 2005
3
0
Aug
Oct
Jan
1979
Apr
1980
Jul
Oct
BLM and experimental streams
Chronic BLM-based copper criteria and macroinvertebrate
effects concentrations: New River at Glen Lyn, VA
Loss of 96% of mayflies, 60% of total
abundance, and 47% of taxa; 42-d
exposure
10-d EC50 (total individuals)
20.0
Dissolved Copper (ug/L)
1997 pH and inorganic data
similar, assuming DOC is
similar
BLM-based chronic criteria (µg/L,
diss.)
25.0
Clements et al., CJFAS.,
1988
10-d EC50 (total individuals)
Clements et al., Aq. Tox.,
1989
15.0
Loss of 96% of mayflies, 60% of total
abundance, and 47% of taxa; 42-d
exposure
10.0
5.0
New River near Blacksburg, VA, New River Valley Bird Club
0.0
23-Aug-96
1-Dec-96
11-Mar-97
19-Jun-97
27-Sep-97
Macroinvertebrate exposures
in August 1987, no DOC data
5-Jan-98
30 week aquatic microcosm experiment
S.F. Hedtke, Aquatic Tox., 1984
1000
BLM-CCC-high
BLM-CCC Low
Diss. Cu (ug/L)
100
Treatments (µg/L)
10
1
0.1
Control
NOEC
LOEC
Severe
Severe
Microcosm community effects
Severe
I think I learned ...
1. BLM performed well across a broad range of waters and with
diverse taxa
2. Paucity of chronic toxicity data from varied waters.
Chemosensory testing valuable, esp. tests of whether effects are
ecologically relevant
3. Experimental stream studies could be compelling
4. BLM too sensitive to DOC?
Assuming 100% of DOC is Cu-reactive may be a factor.
Overprotective at low DOC and underprotective higher DOC.
5. Assuming 50% of DOC is Cu-reactive fulvic acid improved
predictions in most datasets from natural waters.
No datasets were made much worse by the 50% AFA assumption.
6. Adding Mg to the model not helpful in these datasets. Perhaps
limit to site-specific situations where Mg is important.
7. Emphasis on equilibrating waters in FT tests seems misplaced.
8. Quality of DOC and pH measurements critical. Recommend DOC
detection to at least 0.3 mg/L in field data, 0.1 if testing synthetic
waters
References mentioned in the slides:
Besser, J. M., N. Wang, F. J. Dwyer, F. L. Mayer, and C. G. Ingersoll. 2005. Assessing contaminant sensitivity of endangered and threatened
fishes: 2. Chronic toxicity of copper and pentachlorophenol to two endangered species and two surrogate species. Archives of
Environmental Contamination and Toxicology. 48(2): 155-165.
Brooks, P. D., C. M. O’Reilly, S. A. Diamond, D. H. Campbell, R. Knapp, D. Bradford, P. S. Corn, B. Hossack, and K. Tonnessen. 2005. Spatial and
temporal variability in the amount and source of dissolved organic carbon: implications for ultraviolet exposure in amphibian habitats.
Ecosystems. 8(5): 478 - 487.
Chapman, G. A. 1982. Chinook salmon early life stage tests with cadmium, copper, and zinc. Letter of December 6, 1982 to Charles Stephan,
U.S. EPA Environmental Research Laboratory, Duluth. U.S. Environmental Protection Agency, Environmental Research Laboratory,
Corvallis, Oregon (obtained via the USEPA Water Docket, http://www.epa.gov/ow/docket.html).
Clements, W. H., D. S. Cherry, and J. Cairns, Jr. 1988. The impact of heavy metals on macroinvertebrate communities: a comparison of
observational and experimental results. Canadian Journal of Fisheries and Aquatic Sciences. 45(11): 2017-2025.
Clements, W. H., J. L. Farris, D. S. Cherry, and J. Cairns, Jr. 1989. The influence of water quality on macroinvertebrate community responses to
copper in outdoor experimental streams. Aquatic Toxicology. 14(3): 249-262.
Collyard, S. A. 2002. Bioavailability of copper to the amphipod Hyalella azteca. MSc. Department of Zoology and Physiology, University of
Wyoming, Laramie, Wyo.
ENSR. 1996. Development of site-specific water quality criteria for copper in the upper Clark Fork River: Phase III WER Program testing results.
ENSR Consulting and Engineering, 0480-277, Fort Collins, Colo.
Erickson, R. J., D. A. Benoit, V. R. Mattson, H. P. Nelson, and E. N. Leonard. 1996. The effects of water chemistry on the toxicity of copper to
fathead minnows. Environmental Toxicology and Chemistry. 15(2): 181-193.
Geckler, J. R., W. B. Horning, T. M. Nieheisel, Q. H. Pickering, E. L. Robinson, and C. E. Stephan. 1976. Validity of laboratory tests for predicting
copper toxicity in streams. U.S. EPA Ecological Research Service, EPA 600/3-76-116, Cincinnati, OH. 208 pp.
GLEC. 2006. Development of a copper criteria adjustment procedure for Michigan’s Upper Peninsula waters. Great Lakes Environmental Center,
Traverse City, Michigan and Columbia, Ohio, Prepared for the Michigan Department of Environmental Quality. 44 pp.
Hansen, J. A., J. Lipton, P. G. Welsh, J. Morris, D. Cacela, and M. J. Suedkamp. 2002. Relationship between exposure duration, tissue residues,
growth, and mortality in rainbow trout (Oncorhynchus mykiss) juveniles sub-chronically exposed to copper. Aquatic Toxicology. 58: 175188.
Hedtke, S. F. 1984. Structure and function of copper-stressed aquatic microcosms. Aquatic Toxicology. 5(3): 227-244.
Leland, H. V. and J. L. Carter. 1984. Effects of copper on species composition of periphyton in a Sierra Nevada, California, stream. Freshwater
Biology. 14(3): 281-296.
Leland, H. V. and J. L. Carter. 1985. Effects of copper on production of periphyton, nitrogen fixation and processing of leaf litter in a Sierra
Nevada, California, stream. Freshwater Biology. 15(2): 155-173.
Leland, H. V., S. V. Fend, T. L. Dudley, and J. L. Carter. 1989. Effects of copper on species composition of benthic insects in a Sierra Nevada,
California, stream. Freshwater Biology. 21(2): 163-179.
References mentioned in the slides
Maest, A., D. J. Beltman, D. Cacela, J. Lipton, J. Holmes, K. LeJeune, and T. Podrabsky. 1995. Spring 1994 surface water injury assessment
report: Blackbird Mine site NRDA. Submitted by: RCG/Hagler Bailly, Boulder, CO. Submitted to: State of Idaho and National Oceanic
and Atmospheric Administration. 214 pp.
Marr, J. C. A., J. Lipton, D. Cacela, J. A. Hansen, H. L. Bergman, J. S. Meyer, and C. Hogstrand. 1996. Relationship between copper exposure
duration, tissue copper concentration, and rainbow trout growth. Aquatic Toxicology. 36(1): 17-30.
Marr, J. C. A., J. Lipton, D. Cacela, J. A. Hansen, J. S. Meyer, and H. L. Bergman. 1999. Bioavailability and acute toxicity of copper to rainbow
trout (Oncorhynchus mykiss) in the presence of organic acids simulating natural dissolved organic carbon. Canadian Journal of
Fisheries and Aquatic Sciences. 56(8): 1471-1483.
McIntyre, J. K., D. H. Baldwin, J. P. Meador, and N. L. Scholz. 2008. Chemosensory deprivation in juvenile coho salmon exposed to dissolved
copper under varying water chemistry conditions. Environmental Science and Technology. 10.1021/es071603e.
McKim, J. M. and D. A. Benoit. 1971. Effects of long-term exposure to copper on survival, growth and reproduction (Salvelinus fontinalis).
Journal of the Fisheries Research Board of Canada. 28(5): 655-662.
McKim, J. M. and D. A. Benoit. 1974. Duration of toxicity tests for establishing "no effect" concentrations for copper with brook trout
(Salvelinus fontinalis). Journal of the Fisheries Research Board of Canada. 31: 449-452.
Mount, D. I. 1968. Chronic toxicity of copper to fathead minnows (Pimephales promelas, rafinesque) Water Research. 2(3): 215-223.
Santore, R. C., P. R. Paquin, D. M. Di Toro, H. E. Allen, and J. S. Meyer. 2001. Biotic ligand model of the acute toxicity of metals. 2. Application
to acute copper toxicity in freshwater fish and Daphnia. Environmental Toxicology and Chemistry. 20(10): 2397-2402.
Sauter, S., K. S. Buxton, K. J. Macek, and S. R. Petrocelli. 1976. Effects of exposure to heavy metals on selected freshwater fish: toxicity of
copper, cadmium, chromium and lead to eggs and fry of seven fish species. U.S. Environmental Protection Agency, EPA-600/3-76-105,
Duluth, Minnesota. 85 pp.
Schubauer-Berigan, M. K., J. R. Dierkes, P. D. Monson, and G. T. Ankley. 1993. pH-dependent toxicity of Cd, Cu, Ni, Pb, and Zn to Ceriodaphnia
dubia, Pimephales promelas, Hyalella azteca, and Lumbriculus variegatus. Environmental Toxicology and Chemistry. 12(7): 1261-1266.
Seim, W. K., L. R. Curtis, S. W. Glenn, and G. A. Chapman. 1984. Growth and survival of developing steelhead trout (Salmo gairdneri)
continuously or intermittently exposed to copper. Canadian Journal of Fisheries and Aquatic Sciences. 41(3): 433-438.
Stratus. 1996. Preliminary toxicological evaluation, U.S. v. Iron Mountain Mines, Inc. Stratus Consulting, Inc. (formerly Hagler Bailly Services),
Boulder, Colo. http://www.stratusconsulting.com.
Stratus. 1998. Data report: Acute copper toxicity to salmonids in surface waters in the vicinity of the Iron Mountain Mine, California. Stratus
Consulting, Inc. (formerly Hagler Bailly Services), Boulder, Colo. http://www.stratusconsulting.com.
USGS, 2005, National Water Data - NWIS Web: U.S. Geological Survey, Accessed October 2005, http://waterdata.usgs.gov/nwis/
Van Genderen, E. J., A. C. Ryan, J. R. Tomasso, and S. J. Klaine. 2005. Evaluation of acute copper toxicity to larval fathead minnows (Pimephales
promelas) in soft surface waters. Environmental Toxicology and Chemistry. 24(2): 408–414.
Welsh, P. G. 1996. Influence of dissolved organic carbon on the speciation, bioavailability and toxicity of metals to aquatic biota in soft water
lakes. Ph.D., University of Waterloo, Waterloo, Ontario, Canada.
References mentioned in the slides
Welsh, P. G., J. Lipton, T. L. Podrabsky, and G. A. Chapman. 2000. Relative importance of calcium and magnesium in hardness-based
modification of copper toxicity. Environmental Toxicology and Chemistry. 19(6): 1624–1631.
Welsh, P. G., J. L. Parrott, D. G. Dixon, P. V. Hodson, D. J. Spry, and G. Mierle. 1996. Estimating acute copper toxicity to larval fathead minnow
(Pimephales promelas) in soft water from measurements of dissolved organic carbon, calcium, and pH. Canadian Journal of Fisheries
and Aquatic Sciences. 53(6): 1263-1271.
Welsh, P. G., J. F. Skidmore, D. J. Spry, D. G. Dixon, P. V. Hodson, N. J. Hutchinson, and B. E. Hickie. 1993. Effect of pH and dissolved organic
carbon on the toxicity of copper to larval fathead minnow (Pimephales promelas) in natural lake waters of low alkalinity. Canadian
Journal of Fisheries and Aquatic Sciences. 50(7): 1356–1362.