TY - JOUR
T1 - Modes of metal toxicity and impaired branchial ionoregulation in rainbow trout exposed to mixtures of Pb and Cd in soft water
AU - Birceanu, Oana
AU - Chowdhury, M. Jasim
AU - Gillis, Patricia L.
AU - McGeer, James C.
AU - Wood, Chris M.
AU - Wilkie, Michael P.
PY - 2008/9/29
Y1 - 2008/9/29
N2 - Models such as the Biotic Ligand Model (BLM) predict how natural organic matter (NOM) and competing ions (e.g., Ca2+, H+ and Na+) affect metal bioavailability and toxicity in aquatic organisms. However, such models focus upon individual metals, not metal mixtures. This study determined whether Pb and Cd interact at the gill of rainbow trout (Oncorhynchus mykiss) when trout were exposed to environmentally relevant concentrations of these metals (Cd < 100 nmol L-1; Pb < 500 nmol L-1) in soft (<100 μmol Ca2+ L-1), moderately acidic (pH 6.0) water. The 96-h LC50 for Pb was 482 nmol L-1, indicating that Pb was one-order of magnitude more toxic in soft, acidic water than in harder, circumneutral pH waters. The LC50 for Cd alone was also low, 6.7 nmol L-1. Surprisingly, fish acclimated to soft water had multiple populations of Pb-gill and Cd-gill binding sites. A low capacity, high affinity population of Pb-gill binding sites had a Bmax of 18.2 nmol g-1 wet weight (ww) and apparent log KPb-gill = 7.05, but a second low affinity population could not be saturated up to free Pb concentrations approaching 4000 nmol L-1. Two populations of Cd-gill binding sites were characterized: a high affinity, low capacity population with an apparent log KCd-gill = 7.33 and Bmax = 1.73 nmol g-1 ww, and a low affinity, high capacity population with an apparent log KCd-gill = 5.86, and Bmax = 13.7 nmol g-1 ww. At low concentrations, Cd plus Pb accumulation was less than additive because Cd out-competed Pb for gill binding sites, which were likely apical Ca2+-channels. While disturbances to Ca2+ influx were caused by Cd alone, Pb alone had no effect. However, Pb exacerbated Cd-induced disturbances to Ca2+ influx demonstrating that, although Pb- plus Cd-gill binding was less than additive due to competition, the effects (ionic disturbances) were more than additive (synergistic). Pb was also likely binding to intracellular targets, such as branchial carbonic anhydrase, which led to inhibited Na+ influx. This ionic disturbance was exacerbated by Cd. We conclude that exposure to environmentally relevant concentrations of Pb plus Cd results in less than additive metal-gill binding in soft, moderately acidic waters. However, ionic disturbances caused by Cd plus Pb are greater than additive, and this may ultimately increase the toxicity of Cd-Pb mixtures to fishes. Our findings suggest that it may be necessary to re-evaluate water quality criteria and assumptions of the BLM for fish exposed to mixtures of Pb and Cd in the acidic, soft waters found in the Canadian Shield, Scandinavia and other sensitive regions.
AB - Models such as the Biotic Ligand Model (BLM) predict how natural organic matter (NOM) and competing ions (e.g., Ca2+, H+ and Na+) affect metal bioavailability and toxicity in aquatic organisms. However, such models focus upon individual metals, not metal mixtures. This study determined whether Pb and Cd interact at the gill of rainbow trout (Oncorhynchus mykiss) when trout were exposed to environmentally relevant concentrations of these metals (Cd < 100 nmol L-1; Pb < 500 nmol L-1) in soft (<100 μmol Ca2+ L-1), moderately acidic (pH 6.0) water. The 96-h LC50 for Pb was 482 nmol L-1, indicating that Pb was one-order of magnitude more toxic in soft, acidic water than in harder, circumneutral pH waters. The LC50 for Cd alone was also low, 6.7 nmol L-1. Surprisingly, fish acclimated to soft water had multiple populations of Pb-gill and Cd-gill binding sites. A low capacity, high affinity population of Pb-gill binding sites had a Bmax of 18.2 nmol g-1 wet weight (ww) and apparent log KPb-gill = 7.05, but a second low affinity population could not be saturated up to free Pb concentrations approaching 4000 nmol L-1. Two populations of Cd-gill binding sites were characterized: a high affinity, low capacity population with an apparent log KCd-gill = 7.33 and Bmax = 1.73 nmol g-1 ww, and a low affinity, high capacity population with an apparent log KCd-gill = 5.86, and Bmax = 13.7 nmol g-1 ww. At low concentrations, Cd plus Pb accumulation was less than additive because Cd out-competed Pb for gill binding sites, which were likely apical Ca2+-channels. While disturbances to Ca2+ influx were caused by Cd alone, Pb alone had no effect. However, Pb exacerbated Cd-induced disturbances to Ca2+ influx demonstrating that, although Pb- plus Cd-gill binding was less than additive due to competition, the effects (ionic disturbances) were more than additive (synergistic). Pb was also likely binding to intracellular targets, such as branchial carbonic anhydrase, which led to inhibited Na+ influx. This ionic disturbance was exacerbated by Cd. We conclude that exposure to environmentally relevant concentrations of Pb plus Cd results in less than additive metal-gill binding in soft, moderately acidic waters. However, ionic disturbances caused by Cd plus Pb are greater than additive, and this may ultimately increase the toxicity of Cd-Pb mixtures to fishes. Our findings suggest that it may be necessary to re-evaluate water quality criteria and assumptions of the BLM for fish exposed to mixtures of Pb and Cd in the acidic, soft waters found in the Canadian Shield, Scandinavia and other sensitive regions.
KW - Biotic Ligand Model (BLM)
KW - Ca influx
KW - Gills
KW - Metals
KW - Na influx
KW - Toxic Unit Concept
UR - http://www.scopus.com/inward/record.url?scp=51449112131&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=51449112131&partnerID=8YFLogxK
U2 - 10.1016/j.aquatox.2008.07.007
DO - 10.1016/j.aquatox.2008.07.007
M3 - Article
C2 - 18774611
AN - SCOPUS:51449112131
VL - 89
SP - 222
EP - 231
JO - Aquatic Toxicology
JF - Aquatic Toxicology
SN - 0166-445X
IS - 4
ER -