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Very low embryonic crude oil exposures cause lasting cardiac defects in salmon and herring.

Incardona JP, Carls MG, Holland L, Linbo TL, Baldwin DH, Myers MS, Peck KA, Tagal M, Rice SD, Scholz NL - Sci Rep (2015)

Bottom Line: Crude oil disrupts excitation-contraction coupling in fish heart muscle cells, and we show here that salmon and herring exposed as embryos to trace levels of crude oil grow into juveniles with abnormal hearts and reduced cardiorespiratory function, the latter a key determinant of individual survival and population recruitment.The thresholds for developmental cardiotoxicity were remarkably low, suggesting the scale of the Exxon Valdez impact in shoreline spawning habitats was much greater than previously appreciated.Moreover, an irreversible loss of cardiac fitness and consequent increases in delayed mortality in oil-exposed cohorts may have been important contributors to the delayed decline of pink salmon and herring stocks in Prince William Sound.

View Article: PubMed Central - PubMed

Affiliation: Environmental and Fisheries Sciences Division, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA, 2725 Montlake Blvd. E., Seattle, WA 98112.

ABSTRACT
The 1989 Exxon Valdez disaster exposed embryos of pink salmon and Pacific herring to crude oil in shoreline spawning habitats throughout Prince William Sound, Alaska. The herring fishery collapsed four years later. The role of the spill, if any, in this decline remains one of the most controversial unanswered questions in modern natural resource injury assessment. Crude oil disrupts excitation-contraction coupling in fish heart muscle cells, and we show here that salmon and herring exposed as embryos to trace levels of crude oil grow into juveniles with abnormal hearts and reduced cardiorespiratory function, the latter a key determinant of individual survival and population recruitment. Oil exposure during cardiogenesis led to specific defects in the outflow tract and compact myocardium, and a hypertrophic response in spongy myocardium, evident in juveniles 7 to 9 months after exposure. The thresholds for developmental cardiotoxicity were remarkably low, suggesting the scale of the Exxon Valdez impact in shoreline spawning habitats was much greater than previously appreciated. Moreover, an irreversible loss of cardiac fitness and consequent increases in delayed mortality in oil-exposed cohorts may have been important contributors to the delayed decline of pink salmon and herring stocks in Prince William Sound.

No MeSH data available.


Related in: MedlinePlus

Uptake of PAHs into embryos and induction of cyp1a.Individual PAHs measured in water (A,C) and embryos (B,D). (A) Highest exposure concentration for pink salmon embryos (single water sample). (B) Pink salmon embryos at exposure day 21 (single pooled sample, 7 g wet weight). (C) Single exposure concentration for Pacific herring embryo exposure (triplicate water samples, mean ± s.e.m.). (D) Herring embryos at exposure day 8 (mean ± s.e.m.; N = 3 pooled samples, 1–3 g wet weight each). (E) Levels of cyp1a mRNA in herring embryos exposed to gravel effluents measured by QPCR as described under Methods. Data are mean ± s.e.m. of cyp1a levels normalized to ef1α levels measured in two replicates from each treatment with ~150 embryos each. N, naphthalenes; BP, biphenyl; AY, acenaphthylene; AE, acenaphthene; F, fluorenes; D, dibenzothiophenes; P, phenanthrenes; ANT, anthracene; FL, fluoranthene; PY, pyrene; FP, fluoranthenes/pyrenes; BAA, benz[a]anthracene; C, chrysenes; BBF, benzo[b]fluoranthene; BKF, benzo[j]fluoranthene/benzo[k]fluoranthene; BEP, benzo[e]pyrene; BAP, benzo[a]pyrene; PER, perylene; IDY, indeno[1,2,3-cd]pyrene; DBA, dibenz[a,h]anthracene/dibenz[a,c]anthracene; BZP, benzo[ghi]perylene. Parent compound is indicated by a 0 (e.g., N0), while numbers of additional carbons (e.g. methyl groups) for alkylated homologs are indicated as N1, N2, etc.
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f1: Uptake of PAHs into embryos and induction of cyp1a.Individual PAHs measured in water (A,C) and embryos (B,D). (A) Highest exposure concentration for pink salmon embryos (single water sample). (B) Pink salmon embryos at exposure day 21 (single pooled sample, 7 g wet weight). (C) Single exposure concentration for Pacific herring embryo exposure (triplicate water samples, mean ± s.e.m.). (D) Herring embryos at exposure day 8 (mean ± s.e.m.; N = 3 pooled samples, 1–3 g wet weight each). (E) Levels of cyp1a mRNA in herring embryos exposed to gravel effluents measured by QPCR as described under Methods. Data are mean ± s.e.m. of cyp1a levels normalized to ef1α levels measured in two replicates from each treatment with ~150 embryos each. N, naphthalenes; BP, biphenyl; AY, acenaphthylene; AE, acenaphthene; F, fluorenes; D, dibenzothiophenes; P, phenanthrenes; ANT, anthracene; FL, fluoranthene; PY, pyrene; FP, fluoranthenes/pyrenes; BAA, benz[a]anthracene; C, chrysenes; BBF, benzo[b]fluoranthene; BKF, benzo[j]fluoranthene/benzo[k]fluoranthene; BEP, benzo[e]pyrene; BAP, benzo[a]pyrene; PER, perylene; IDY, indeno[1,2,3-cd]pyrene; DBA, dibenz[a,h]anthracene/dibenz[a,c]anthracene; BZP, benzo[ghi]perylene. Parent compound is indicated by a 0 (e.g., N0), while numbers of additional carbons (e.g. methyl groups) for alkylated homologs are indicated as N1, N2, etc.

Mentions: Salmon and herring embryos were exposed to water-soluble components of ANSCO using oil-coated gravel generator columns, beginning shortly after fertilization and ending within the organogenesis phase after completion of key steps of early heart development (~60% of embryogenesis, Supplementary Fig. S1). For salmon, initial aqueous ΣPAH concentrations were linearly related to nominal oil load (Supplementary Fig. S2A), resulting in an exposure range of 0.2  μg/L (control) through 45.4  μg/L (Table 1), with an exponential drop in ΣPAH concentrations for all oil treatments during exposure (Supplementary Fig. S2B). For herring, column flow was initiated three weeks before embryo exposure started, and initial aqueous ΣPAH concentrations were 0.230 ± 0.010  μg/L and 0.039 ± 0.003  μg/L for oiled and clean gravel, respectively (Table 1). More prolonged weathering (relative to the salmon exposure) was evident as a greater depletion of parent and C1-naphthalenes, fluorenes, dibenzothiophenes, and phenanthrenes, with higher proportions of C2-alkyl homologs (Fig. 1C). In general embryos of both species accumulated patterns of individual PAHs that mirrored the PAH composition of water (Fig. 1 and Supplementary Fig. S3). Pink salmon embryos accumulated PAHs in a concentration-dependent manner (Supplementary Fig. S3), with tissue ΣPAH levels ranging from 26 ng/g wet weight (control) to 2474 ng/g (Table 1), while herring embryos accumulated ΣPAH concentrations of 28.6 ± 10.2 ng/g wet weight and 9.3 ± 3.7 ng/g wet weight from oiled and control gravel effluent, respectively (Table 1, Fig. 1D). This very low level PAH exposure in herring was nevertheless sufficient to cause a 5-fold induction of cyp1a mRNA, encoding the PAH-metabolizing enzyme cytochrome P4501A (Fig. 1E).


Very low embryonic crude oil exposures cause lasting cardiac defects in salmon and herring.

Incardona JP, Carls MG, Holland L, Linbo TL, Baldwin DH, Myers MS, Peck KA, Tagal M, Rice SD, Scholz NL - Sci Rep (2015)

Uptake of PAHs into embryos and induction of cyp1a.Individual PAHs measured in water (A,C) and embryos (B,D). (A) Highest exposure concentration for pink salmon embryos (single water sample). (B) Pink salmon embryos at exposure day 21 (single pooled sample, 7 g wet weight). (C) Single exposure concentration for Pacific herring embryo exposure (triplicate water samples, mean ± s.e.m.). (D) Herring embryos at exposure day 8 (mean ± s.e.m.; N = 3 pooled samples, 1–3 g wet weight each). (E) Levels of cyp1a mRNA in herring embryos exposed to gravel effluents measured by QPCR as described under Methods. Data are mean ± s.e.m. of cyp1a levels normalized to ef1α levels measured in two replicates from each treatment with ~150 embryos each. N, naphthalenes; BP, biphenyl; AY, acenaphthylene; AE, acenaphthene; F, fluorenes; D, dibenzothiophenes; P, phenanthrenes; ANT, anthracene; FL, fluoranthene; PY, pyrene; FP, fluoranthenes/pyrenes; BAA, benz[a]anthracene; C, chrysenes; BBF, benzo[b]fluoranthene; BKF, benzo[j]fluoranthene/benzo[k]fluoranthene; BEP, benzo[e]pyrene; BAP, benzo[a]pyrene; PER, perylene; IDY, indeno[1,2,3-cd]pyrene; DBA, dibenz[a,h]anthracene/dibenz[a,c]anthracene; BZP, benzo[ghi]perylene. Parent compound is indicated by a 0 (e.g., N0), while numbers of additional carbons (e.g. methyl groups) for alkylated homologs are indicated as N1, N2, etc.
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Show All Figures
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f1: Uptake of PAHs into embryos and induction of cyp1a.Individual PAHs measured in water (A,C) and embryos (B,D). (A) Highest exposure concentration for pink salmon embryos (single water sample). (B) Pink salmon embryos at exposure day 21 (single pooled sample, 7 g wet weight). (C) Single exposure concentration for Pacific herring embryo exposure (triplicate water samples, mean ± s.e.m.). (D) Herring embryos at exposure day 8 (mean ± s.e.m.; N = 3 pooled samples, 1–3 g wet weight each). (E) Levels of cyp1a mRNA in herring embryos exposed to gravel effluents measured by QPCR as described under Methods. Data are mean ± s.e.m. of cyp1a levels normalized to ef1α levels measured in two replicates from each treatment with ~150 embryos each. N, naphthalenes; BP, biphenyl; AY, acenaphthylene; AE, acenaphthene; F, fluorenes; D, dibenzothiophenes; P, phenanthrenes; ANT, anthracene; FL, fluoranthene; PY, pyrene; FP, fluoranthenes/pyrenes; BAA, benz[a]anthracene; C, chrysenes; BBF, benzo[b]fluoranthene; BKF, benzo[j]fluoranthene/benzo[k]fluoranthene; BEP, benzo[e]pyrene; BAP, benzo[a]pyrene; PER, perylene; IDY, indeno[1,2,3-cd]pyrene; DBA, dibenz[a,h]anthracene/dibenz[a,c]anthracene; BZP, benzo[ghi]perylene. Parent compound is indicated by a 0 (e.g., N0), while numbers of additional carbons (e.g. methyl groups) for alkylated homologs are indicated as N1, N2, etc.
Mentions: Salmon and herring embryos were exposed to water-soluble components of ANSCO using oil-coated gravel generator columns, beginning shortly after fertilization and ending within the organogenesis phase after completion of key steps of early heart development (~60% of embryogenesis, Supplementary Fig. S1). For salmon, initial aqueous ΣPAH concentrations were linearly related to nominal oil load (Supplementary Fig. S2A), resulting in an exposure range of 0.2  μg/L (control) through 45.4  μg/L (Table 1), with an exponential drop in ΣPAH concentrations for all oil treatments during exposure (Supplementary Fig. S2B). For herring, column flow was initiated three weeks before embryo exposure started, and initial aqueous ΣPAH concentrations were 0.230 ± 0.010  μg/L and 0.039 ± 0.003  μg/L for oiled and clean gravel, respectively (Table 1). More prolonged weathering (relative to the salmon exposure) was evident as a greater depletion of parent and C1-naphthalenes, fluorenes, dibenzothiophenes, and phenanthrenes, with higher proportions of C2-alkyl homologs (Fig. 1C). In general embryos of both species accumulated patterns of individual PAHs that mirrored the PAH composition of water (Fig. 1 and Supplementary Fig. S3). Pink salmon embryos accumulated PAHs in a concentration-dependent manner (Supplementary Fig. S3), with tissue ΣPAH levels ranging from 26 ng/g wet weight (control) to 2474 ng/g (Table 1), while herring embryos accumulated ΣPAH concentrations of 28.6 ± 10.2 ng/g wet weight and 9.3 ± 3.7 ng/g wet weight from oiled and control gravel effluent, respectively (Table 1, Fig. 1D). This very low level PAH exposure in herring was nevertheless sufficient to cause a 5-fold induction of cyp1a mRNA, encoding the PAH-metabolizing enzyme cytochrome P4501A (Fig. 1E).

Bottom Line: Crude oil disrupts excitation-contraction coupling in fish heart muscle cells, and we show here that salmon and herring exposed as embryos to trace levels of crude oil grow into juveniles with abnormal hearts and reduced cardiorespiratory function, the latter a key determinant of individual survival and population recruitment.The thresholds for developmental cardiotoxicity were remarkably low, suggesting the scale of the Exxon Valdez impact in shoreline spawning habitats was much greater than previously appreciated.Moreover, an irreversible loss of cardiac fitness and consequent increases in delayed mortality in oil-exposed cohorts may have been important contributors to the delayed decline of pink salmon and herring stocks in Prince William Sound.

View Article: PubMed Central - PubMed

Affiliation: Environmental and Fisheries Sciences Division, Northwest Fisheries Science Center, National Marine Fisheries Service, NOAA, 2725 Montlake Blvd. E., Seattle, WA 98112.

ABSTRACT
The 1989 Exxon Valdez disaster exposed embryos of pink salmon and Pacific herring to crude oil in shoreline spawning habitats throughout Prince William Sound, Alaska. The herring fishery collapsed four years later. The role of the spill, if any, in this decline remains one of the most controversial unanswered questions in modern natural resource injury assessment. Crude oil disrupts excitation-contraction coupling in fish heart muscle cells, and we show here that salmon and herring exposed as embryos to trace levels of crude oil grow into juveniles with abnormal hearts and reduced cardiorespiratory function, the latter a key determinant of individual survival and population recruitment. Oil exposure during cardiogenesis led to specific defects in the outflow tract and compact myocardium, and a hypertrophic response in spongy myocardium, evident in juveniles 7 to 9 months after exposure. The thresholds for developmental cardiotoxicity were remarkably low, suggesting the scale of the Exxon Valdez impact in shoreline spawning habitats was much greater than previously appreciated. Moreover, an irreversible loss of cardiac fitness and consequent increases in delayed mortality in oil-exposed cohorts may have been important contributors to the delayed decline of pink salmon and herring stocks in Prince William Sound.

No MeSH data available.


Related in: MedlinePlus