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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

Dose-dependent changes in juvenile salmon cardiac morphology following embryonic oil exposure.Anatomical locations of measurements are shown in Supplementary Fig. S7. (A) Ventricular length and width normalized to fish fork length measured in juveniles 8 months after exposure (mean ± s.e.m.). Data were fit to a linear regression model; P value indicates significance of the slope. (B) Ventricular aspect ratio measured in juveniles 8 months (triangles) and 10 months (diamonds) after exposure, and both age groups pooled (circles) fit a linear regression model (mean ± s.e.m). P values indicate significance of slope. (C) Length of the bulbus arteriosus normalized to ventricular length in juveniles 8 months after exposure (mean ± s.e.m.). Data did not fit linear or non-linear regression models, but were highly significant by ANOVA (P = 0.0012); asterisks indicate doses significantly different from control (Dunnett’s test, α = 0.05). (D) Outflow tract angle in juveniles 8 months following exposure (mean ± s.e.m.). For 8 month fish, N = 12 for all oil exposed groups, 13 for control; for 10 month fish, N = 20–23 for all groups except lowest oil exposure dose, N = 11.
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f3: Dose-dependent changes in juvenile salmon cardiac morphology following embryonic oil exposure.Anatomical locations of measurements are shown in Supplementary Fig. S7. (A) Ventricular length and width normalized to fish fork length measured in juveniles 8 months after exposure (mean ± s.e.m.). Data were fit to a linear regression model; P value indicates significance of the slope. (B) Ventricular aspect ratio measured in juveniles 8 months (triangles) and 10 months (diamonds) after exposure, and both age groups pooled (circles) fit a linear regression model (mean ± s.e.m). P values indicate significance of slope. (C) Length of the bulbus arteriosus normalized to ventricular length in juveniles 8 months after exposure (mean ± s.e.m.). Data did not fit linear or non-linear regression models, but were highly significant by ANOVA (P = 0.0012); asterisks indicate doses significantly different from control (Dunnett’s test, α = 0.05). (D) Outflow tract angle in juveniles 8 months following exposure (mean ± s.e.m.). For 8 month fish, N = 12 for all oil exposed groups, 13 for control; for 10 month fish, N = 20–23 for all groups except lowest oil exposure dose, N = 11.

Mentions: In addition to reducing swimming performance (and by proxy, aerobic capacity) in both species, embryonic oil exposure affected the eventual shape of the ventricle and outflow tract in juvenile hearts (Supplementary Fig. S6). Morphology of juvenile salmon ventricles was assessed after eight and ten months of growth in clean water. At eight months, there was a significant, ΣPAH dose-dependent increase in normalized ventricle length (R2 = 0.83, P = 0.03; Fig. 3A) but not width (R2 = 0.27, P = 0.4), resulting in a significant increase in ventricular aspect ratio (Fig. 3B; R2 = 0.96, P = 0.003). This persisted to ten months post-exposure (Fig. 3B), albeit with weaker significance (R2 = 0.76, P = 0.055). The length of the bulbus arteriosus (normalized to ventricular length) was reduced by oil exposure (Fig. 3C). Although not clearly dose-dependent, the effect of oil exposure was highly significant (ANOVA P = 0.0012) with salmon from all oil treatments having shorter outflow tracts relative to controls (all P values < 0.005) except for the lowest ΣPAH exposure (9.8  μg/L). While measurements of the outflow tract angle had greater variability, there was a clear trend that mirrored the effect on bulbus arteriosus length (Fig. 3D). Absolute dimensions of the ventricle were not significantly altered by oil exposure in a dose-dependent manner. Despite overall smaller body sizes in exposed fish, their ventricles tended to be larger than controls, with only the 30  μg/L exposure (12  μg/g tissue ΣPAH) group showing a significant increase in absolute length at 3.46 ± 0.08 mm relative to 2.96 ± 0.09 mm in controls (Supplementary Fig. S7). There were no significant differences in absolute width.


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)

Dose-dependent changes in juvenile salmon cardiac morphology following embryonic oil exposure.Anatomical locations of measurements are shown in Supplementary Fig. S7. (A) Ventricular length and width normalized to fish fork length measured in juveniles 8 months after exposure (mean ± s.e.m.). Data were fit to a linear regression model; P value indicates significance of the slope. (B) Ventricular aspect ratio measured in juveniles 8 months (triangles) and 10 months (diamonds) after exposure, and both age groups pooled (circles) fit a linear regression model (mean ± s.e.m). P values indicate significance of slope. (C) Length of the bulbus arteriosus normalized to ventricular length in juveniles 8 months after exposure (mean ± s.e.m.). Data did not fit linear or non-linear regression models, but were highly significant by ANOVA (P = 0.0012); asterisks indicate doses significantly different from control (Dunnett’s test, α = 0.05). (D) Outflow tract angle in juveniles 8 months following exposure (mean ± s.e.m.). For 8 month fish, N = 12 for all oil exposed groups, 13 for control; for 10 month fish, N = 20–23 for all groups except lowest oil exposure dose, N = 11.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4561892&req=5

f3: Dose-dependent changes in juvenile salmon cardiac morphology following embryonic oil exposure.Anatomical locations of measurements are shown in Supplementary Fig. S7. (A) Ventricular length and width normalized to fish fork length measured in juveniles 8 months after exposure (mean ± s.e.m.). Data were fit to a linear regression model; P value indicates significance of the slope. (B) Ventricular aspect ratio measured in juveniles 8 months (triangles) and 10 months (diamonds) after exposure, and both age groups pooled (circles) fit a linear regression model (mean ± s.e.m). P values indicate significance of slope. (C) Length of the bulbus arteriosus normalized to ventricular length in juveniles 8 months after exposure (mean ± s.e.m.). Data did not fit linear or non-linear regression models, but were highly significant by ANOVA (P = 0.0012); asterisks indicate doses significantly different from control (Dunnett’s test, α = 0.05). (D) Outflow tract angle in juveniles 8 months following exposure (mean ± s.e.m.). For 8 month fish, N = 12 for all oil exposed groups, 13 for control; for 10 month fish, N = 20–23 for all groups except lowest oil exposure dose, N = 11.
Mentions: In addition to reducing swimming performance (and by proxy, aerobic capacity) in both species, embryonic oil exposure affected the eventual shape of the ventricle and outflow tract in juvenile hearts (Supplementary Fig. S6). Morphology of juvenile salmon ventricles was assessed after eight and ten months of growth in clean water. At eight months, there was a significant, ΣPAH dose-dependent increase in normalized ventricle length (R2 = 0.83, P = 0.03; Fig. 3A) but not width (R2 = 0.27, P = 0.4), resulting in a significant increase in ventricular aspect ratio (Fig. 3B; R2 = 0.96, P = 0.003). This persisted to ten months post-exposure (Fig. 3B), albeit with weaker significance (R2 = 0.76, P = 0.055). The length of the bulbus arteriosus (normalized to ventricular length) was reduced by oil exposure (Fig. 3C). Although not clearly dose-dependent, the effect of oil exposure was highly significant (ANOVA P = 0.0012) with salmon from all oil treatments having shorter outflow tracts relative to controls (all P values < 0.005) except for the lowest ΣPAH exposure (9.8  μg/L). While measurements of the outflow tract angle had greater variability, there was a clear trend that mirrored the effect on bulbus arteriosus length (Fig. 3D). Absolute dimensions of the ventricle were not significantly altered by oil exposure in a dose-dependent manner. Despite overall smaller body sizes in exposed fish, their ventricles tended to be larger than controls, with only the 30  μg/L exposure (12  μg/g tissue ΣPAH) group showing a significant increase in absolute length at 3.46 ± 0.08 mm relative to 2.96 ± 0.09 mm in controls (Supplementary Fig. S7). There were no significant differences in absolute width.

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