Re-analysis of existing uranium freshwater chronic toxicity

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SUPPLEMENTAL DATA
Table S1 Chronology of uranium chronic toxicity studies for freshwater species, which report
concentration-response relationships based on ecologically relevant endpoints (e.g. growth,
development, reproduction, survival).
Species
Reference1
Test type, toxicity measure reported
Peer-reviewed studies
Pre 2000
Daphnia magna
21-d survival / reproduction, NOEC
Poston et al. (1984)
Hydra viridissima
96-h population growth rate, NOEC
Hyne et al. (1992)
Melanotaenia splendida
inornata
7-d survival, NOEC
Holdway (1992)
Mogurnda mogurnda
7-d (+ 7-d post-exposure) survival, NOEC
Holdway (1992)
Moinodaphnia macleayi
5-d survival, NOEC
H. viridissima
96-h population growth rate, BEC10
Markich and Camilleri (1997)
H. viridissima
96-h population growth rate, BEC10
Riethmuller et al. (2000)
Chlorella sp. 1
72-h cell division rate, BEC10
Franklin et al. (2000)
Chlorella sp. 2
72-h cell division rate, BEC10
Charles et al. (2002)
Lemna gibba
21-d growth rate, NOEC
M. macleayi
3 brood reproduction, NOEC
Hyne et al. (1993)
2000 – present
Mkandawire and Dudel (2002)
Semaan et al. (2001)
Catostomus commersoni 30-d growth, NOEC
Liber et al. (2004a)
Chlorella sp. 1
72-h cell division rate, NOEC
Hogan et al. (2005)
Lemna aequinoctialis
96-h population growth rate, MDEC
Charles et al. (2006)
D. magna
21-d growth / reproduction, NOEC / EC10
Zeman et al. (2008)
Danio rerio
15-d development / growth, NOEC
L. aequinoctialis
96-h population growth rate, NOEC / IC10
Hogan et al. (2010)
Amerianna cumingi
96-h egg production, NOEC / IC10
Hogan et al. (2010)
D. magna
Multigeneration, growth/reproduction, NOEC
M. mogurnda
28-d growth / survival, IC10
Cheng et al. (2010)
Chlorella sp. 1
72-h cell division rate, IC50
Trenfield et al. (2011)
H. viridissima
96-h population growth rate, IC50
Trenfield et al. (2011)
Euglena gracilis
96-h cell division rate, IC50
Trenfield et al. (2012)
Bourrachot et al. (2008)
Massarin et al. (2010)
Non peer-reviewed studies2
Pre 2000
Ceriodaphnia dubia
2000 – present
7-d (3 brood) reproduction, NOEC
Pickett et al. (1993)
2
1
Salvelinus namaycush
141-d development / survival, NOEC
Liber et al. (2004b)
Selenastrum
capricornutum /
Pseudokirchneriella
subcapitata
72-h cell division rate, IC25 / IC50 / NOEC
Vizon SciTec Inc. (2004)
Lemna minor
7-d growth, IC25 / IC50
Vizon SciTec Inc. (2004)
C. dubia
7-d (3 brood) reproduction, IC25 / IC50 /
NOEC
Vizon SciTec Inc. (2004)
Hyalella azteca
14-d survival / growth
Vizon SciTec Inc. (2004)
Oncorhynchus mykiss
30-d hatching / viability
Vizon SciTec Inc. (2004)
Esox lucius
65-d development / growth / survival, NOEC
Liber et al. (2005)
S. capricornutum / P.
subcapitata
72-h cell division rate, IC25 / IC50 / NOEC
Liber et al. (2007)
Chlamydomonsa
reinhardtii
72-h cell division rate, IC25 / IC50 / NOEC
Liber et al. (2007)
Cryptomonas erosa
6-d cell division rate, IC25 / IC50 / NOEC
Liber et al. (2007)
D. magna
21-d reproduction, IC25 / IC50 /
NOEC
Liber et al. (2007)
C. dubia
7-d (3 brood) reproduction, IC25 / IC50 / NOEC
Liber et al. (2007)
Simocephalus
serrulatus
21-d reproduction, IC25 / IC50 /
NOEC
Liber et al. (2007)
Chironomus tentans
28-d survival / growth / emergence, IC25 / IC50
/ NOEC
Liber et al. (2007)
Corynoneura spp.
28-d survival / emergence, IC25 / IC50 / NOEC
Liber et al. (2007)
H. azteca
28-d survival / growth, IC25 / IC50 / NOEC
Liber et al. (2007)
See reference list below for details.
2
Non peer-reviewed studies were included where they have been cited in the peer-reviewed literature
and they did not present research subsequently published in peer-reviewed publications.
References for Table S1
Bourrachot S, Simon O, Gilbin R. 2008. The effects of waterborne uranium on the hatching success,
development, and survival of early life stages of zebrafish (Danio rerio). Aquat Toxicol 90:29-36.
Charles A, Markich S, Stauber J, de Filippis L. 2002. The effect of water hardness on the toxicity of
uranium to a tropical freshwater alga (Chlorella sp.). Aquat Toxicol 60:61-73.
Charles AL, Markich, Scott J and Ralph P. 2006. Toxicity of uranium and copper individually, and in
combination, to a tropical freshwater macrophyte Lemna aequinoctialis. Chemosphere 62:12241233.
3
Cheng KL, Hogan AC, Parry DL, Markich SJ, Harford AJ, van Dam RA. 2010. Uranium toxicity and
speciation during chronic exposure to the tropical freshwater fish, Mogurnda mogurnda.
Chemosphere 79:547-554.
Franklin NM, Stauber JL, Markich SJ, Lim RP. 2000. pH-dependent toxicity of copper and uranium
to a tropical freshwater alga (Chlorella sp.). Aquat Toxicol 48:275-289.
Hogan AC, van Dam RA, Markich SJ, Camilleri C. 2005. Chronic toxicity of uranium to a tropical
green alga (Chlorella sp.) in natural waters and the influence of dissolved organic carbon. Aquat
Toxicol 75:343-353.
Hogan A, van Dam RA, Houston MA, Harford AJ, Nou S. 2010. Uranium exposure to the tropical
duckweed Lemna aequinoctialis and pulmonate snail Amerianna cumingi: fate and toxicity. Arch
Environ Contam Toxicol 59:204-215.
Holdway DA. 1992. Uranium toxicity to two species of Australian tropical fish. Sci Total Environ
125:137-158.
Hyne RV, Rippon GD, Ellender G. 1992. pH-dependent uranium toxicity to freshwater hydra. Sci
Total Environ 125:159-173.
Hyne RV, Padovan A, Parry DL, Renaud SM. 1993. Increased fecundity of the cladoceran
Moinodaphnia macleayi on a diet supplemented with a green alga, and its use in uranium toxicity
tests. Aust J Mar Fresh Res 44:389-399.
Liber K, Stoughton S, Rosaasen A. 2004a. Chronic uranium toxicity to White Sucker fry (Catostomus
commersoni) Bull Environ Contam Toxicol 73: 1065-1071.
Liber K, Stoughton S, Janz D. 2004b. Uranium toxicity to early life-stage lake trout (Salvelinus
namaycush). Report for Saskatchewan Environment, Shield EcoRegion-Uranium Mining Unit,
Prepared by the Toxicology Centre, University of Saskatchewan, Saskatoon, Canada.
4
Liber K, Stoughton S, Janz D. 2005. Uranium toxicity to early life-stage northern pike (Esox lucius).
Report for Saskatchewan Environment, Shield EcoRegion-Uranium Mining Unit, Saskatoon,
Canada. Prepared by the Toxicology Centre, University of Saskatchewan, Saskatoon, SK, Canada.
Liber K, deRosemond S, Budnick K. 2007. Uranium toxicity to regionally-representative algae and
invertebrate species. Saskatoon, SK, submitted to AREVA Resources Inc. and Cameco
Corporation, final report.
Markich SJ, Camilleri C. 1997. Investigation of metal toxicity to tropical biota: Recommendations for
revision of the Australian water quality guidelines. Supervising Scientist Report 127. Supervising
Scientist, Department of Sustainability, Environment, Water, Population and Communities,
Darwin, Australia.
Pickett JB, Specht WL, Keyes JL. 1993. Acute and chronic toxicity of uranium compounds to
Ceriodaphnia dubia, Rep. No. WSRC-RP-92-995. Prepared by the Department of Energy under
contract DE-AC09-89SR 18035.
Poston TM, Hanf RW, Simmons MA. 1984. Toxicity of uranium to Daphnia magna. Water Air Soil
Poll 22:289-298.
Massarin S, Alonzo F, Garcia-Sanchez L, Gilbin R, Garnier-Laplace J, Poggiale J. 2010. Effects of
chronic uranium exposure on life history and physiology of Daphnia magna over three successive
generations. Aquat Toxicol 99:309-319.
Mkandawire M, Dudel GE. 2002. Uranium attenuation from tailing waters by floating macrophyte
Lemna gibba L. In Merkel JB, Planer-Friedrich B, Wolkersdorfer C, eds, Uranium in the aquatic
environment Berlin, Springer: 623-630.
Riethmuller N, Markich S, Parry D, van Dam R. 2000. The effect of true water hardness and
alkalinity on the toxicity of Cu and U to two tropical Australian freshwater organisms. Supervising
Scientist Report 155. Supervising Scientist, Department of Sustainability, Environment, Water,
Population and Communities, Darwin, Australia.
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Semaan M, Holdway DA, Van Dam R. 2001. Comparative sensitivity of three populations of the
cladoceran Moinodaphnia macleayi to acute and chronic uranium exposure. Environ Toxicol
16:365-376.
Trenfield MA, Ng JC, Noller BN, Markich SJ, Van Dam RA. 2011. Dissolved organic carbon reduces
uranium bioavailability and toxicity. 2. Uranium[VI] speciation and toxicity to three tropical
freshwater organisms. Environ Sci Technol 45:3082-3089.
Trenfield MA, Ng JC, Noller BN, Markich SJ, van Dam RA. 2012. Dissolved organic carbon reduces
uranium toxicity to the unicellular eukaryote Euglena gracilis. Ecotoxicology 21:1013-1023.
Vizon SciTec Inc. 2004. Final report on the toxicity investigation of uranium to aquatic organisms.
CNSC Project No.: R205.1.
Zeman FA, Gilbin R, Alonzo F, Lecomte-Pradines C, Garnier-Laplace J, Aliaume C. 2008. Effects of
waterborne uranium on survival, growth, reproduction and physiological processes of the
freshwater cladoceran Daphnia magna. Aquat Toxicol 86:370-378.
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Table S2 Stepwise regression relationships between toxicity measures for uranium and key physico-chemical variables, for Chlorella spp.,
Hydra viridissima, and both species combined.
Species / toxicity Predictor
measure
Model equation
Model details
(r2, P)
Chlorella spp. (n = 20)
IC10
DOC
IC10 = 36.24 + 10.4[DOC]
0.68, <0.001
IC50
DOC
IC50 = 74.10 + 21.0[DOC]
0.74, <0.001
DOC, hardness
IC50 = 53.58 + 22.6[DOC] + 0.44[hardness]
0.82, <0.001 (DOC), 0.008 (hardness)
Hydra viridissima (n = 14)
IC10
DOC
IC10 = 50.31 + 7.4[DOC]
0.48, 0.004
IC50
DOC
IC50 = 103.74 + 16.4[DOC]
0.59, 0.001
IC10
DOC
IC10 = 42.58 + 9.0[DOC]
0.62, <0.001
IC50
DOC
IC50 = 87.35 + 18.9[DOC]
0.68, <0.001
DOC, hardness
IC50 = 60.77 + (21.0[DOC]) + (0.47[hardness])
0.79, <0.001 (DOC), <0.001 (hardness)
Combined (n = 34)
7
A.
B.
120
pH 5.7
pH 6.5
100
Percent of control growth rate
Percent of control growth rate
120
80
60
40
20
0
0 mg/L DOC
2.6 mg/L DOC
3.4 mg/L DOC
4.1 mg/L DOC
8.1 mg/L DOC
100
80
60
40
20
0
0
50
100
150
200
250
300
0
100
Uranium ( g/L)
200
300
400
Uranium ( g/L)
C.
Percent of control growth rate
120
0 mg/L DOC
1.0 mg/L DOC
5.1 mg/L DOC
10.2 mg/L DOC
20.4 mg/L DOC
100
80
60
40
20
0
0
200
400
600
800
1000
1200
1400
1600
Uranium (µg/L)
D.
E.
120
0 mg/L DOC
1.0 mg/L DOC
4.7 mg/L DOC
9.5 mg/L DOC
100
Percent of control growth rate
Percent of control growth rate
120
80
60
40
20
0
8 mg/L hardness
40 mg/L hardness
100 mg/L hardness
400 mg/L hardness
100
80
60
40
20
0
0
100
200
300
400
500
600
0
100
200
Uranium ( g/L)
300
400
500
600
700
Uranium ( g/L)
Figure S1 Concentration-response plots for uranium toxicity to Chlorella sp. 1 based on data from (A) Franklin
et al. [18], individual replicates plotted; (B) Hogan et al. [19], individual replicates plotted; (C) Trenfield et al.
[20], Suwannee River Fulvic Acid as the DOC source; means  standard error; and (D) Trenfield et al. [20],
Sandy Billabong DOC as the DOC source; means  standard error; and Chlorella sp. 2 based on data from (E)
Charles et al. [21], means  standard error. Model details are presented in Table 1.
800
8
A.
B.
120
Percent of control growth rate
Percent of control growth rate
120
100
80
60
40
20
Dry season
Wet season
0
0
100
80
60
40
20
0
100
200
300
400
0
200
Uranium ( g/L)
400
C.
1000
1200
120
6.6 mg/L hardness
165 mg/L hardness
330 mg/L hardness
100
Percent of control growth rate
Percent of control growth rate
800
D.
120
80
60
40
20
0
100
80
60
40
20
0
0
200
400
600
800
1000
1200
0
100
Uranium ( g/L)
200
300
400
500
600
Uranium ( g/L)
E.
F.
120
0 mg/L DOC
0.9 mg/L DOC
4.9 mg/L DOC
9.7 mg/L DOC
19.5 mg/L DOC
100
80
60
40
20
0
Percent of control growth rate
120
Percent of control growth rate
600
Uranium ( g/L)
0 mg/L DOC
0.9 mg/L DOC
4.8 mg/L DOC
9.7 mg/L DOC
100
80
60
40
20
0
0
200
400
600
Uranium (µg/L)
800
1000
0
100
200
300
400
500
600
Uranium (µg/L)
Figure S2 Concentration-response plots for uranium toxicity to Hydra viridissima based on data from (A) Hyne
et al. [22], means  standard error for dry season, means only for wet season; (B) Markich & Camilleri [23],
means  standard error; (C) Riethmuller et al. [24], means  standard error; (D) Riethmuller et al. [24], means 
standard error; data for water hardness and alkalinity of 165 mg/L and 102 mg/L (as CaCO 3), respectively; (E)
Trenfield et al. [20], Suwannee River Fulvic Acid as the DOC source; means  standard error; and (F) Trenfield
et al. [20], Sandy Billabong DOC as the DOC source; means  standard error. Model details are presented in
9
Table 2.
10
A.
B.
120
Test 1
Test 2
Test 3
Test 4
100
80
Percent of control survival
Percent of control reproduction
120
60
40
20
100
80
60
40
20
0
0
0
20
40
60
80
100
0
120
50
100
C.
200
D.
120
Percent of control reproduction
120
Percent of control reproduction
150
Uranium ( g/L)
Uranium ( g/L)
100
80
60
40
Laboratory population (Test 1)
Laboratory population (Test 2)
Laboratory population (Test 3)
20
0
100
80
60
40
20
Wild population (Test 1)
Wild population (Test 2)
0
0
10
20
30
Uranium ( g/L)
40
50
0
10
20
30
40
50
Uranium ( g/L)
Figure S3 Concentration-response plots for uranium toxicity to Moinodaphnia macleayi based on data from (A)
unpublished data from the Environmental Research Institute of the Supervising Scientist from tests undertaken
in 1992, means  standard error; (B) Hyne et al. [25], means  standard error; survival data; (C) Semaan et al.
[26], means  standard error; tests using an established laboratory population; and (D) Semaan et al. [26], means
 standard error; tests using a wild population. Model details are presented in Table 3.
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