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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

Embryonic oil exposure reduced critical swimming speed and maximum metabolic rate of juveniles.Mean Ucrit (±s.e.m.) is given as an absolute speed (A and C, cm/s) or relative to body length (B and D, BL/s) for (A,B) salmon exposed to clean effluent (ΣPAH 0.2  μg/L, N = 51) or oiled gravel effluent with ΣPAH 15  μg/L (N = 45) and 45  μg/L (N = 52); and (C,D) herring exposed to clean gravel effluent (ΣPAH 0.04  μg/L, N = 32) and oiled gravel effluent with ΣPAH 0.23  μg/L (N = 33). (E) Maximum metabolic rate (MMR) for juvenile herring during Ucrit assays. Oxygen consumption data passing statistical criteria (clean gravel, N = 23; oiled gravel, N = 22) were used to calculate MMR as described under Methods. For salmon data, P values are shown for effect of oil exposure from ANOVA while P values over oil-exposed groups represent comparison to controls in post-hoc analysis. For herring data, P values shown are for effect of treatment (oil exposure) and tank effect, respectively, from a nested ANOVA (replicate nested under treatment).
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f2: Embryonic oil exposure reduced critical swimming speed and maximum metabolic rate of juveniles.Mean Ucrit (±s.e.m.) is given as an absolute speed (A and C, cm/s) or relative to body length (B and D, BL/s) for (A,B) salmon exposed to clean effluent (ΣPAH 0.2  μg/L, N = 51) or oiled gravel effluent with ΣPAH 15  μg/L (N = 45) and 45  μg/L (N = 52); and (C,D) herring exposed to clean gravel effluent (ΣPAH 0.04  μg/L, N = 32) and oiled gravel effluent with ΣPAH 0.23  μg/L (N = 33). (E) Maximum metabolic rate (MMR) for juvenile herring during Ucrit assays. Oxygen consumption data passing statistical criteria (clean gravel, N = 23; oiled gravel, N = 22) were used to calculate MMR as described under Methods. For salmon data, P values are shown for effect of oil exposure from ANOVA while P values over oil-exposed groups represent comparison to controls in post-hoc analysis. For herring data, P values shown are for effect of treatment (oil exposure) and tank effect, respectively, from a nested ANOVA (replicate nested under treatment).

Mentions: We used critical swimming speed (Ucrit) as a measure of cardiorespiratory performance in juvenile pink salmon and Pacific herring. Ucrit is the maximum sustained swimming speed reached at the point of fatigue and at which maximum sustained oxygen uptake occurs22. A swim tunnel respirometer designed for small fish (4–12 g) was used to measure Ucrit for both species at 8–9° C following seven to eight months of growth in clean water. For both species, Ucrit was significantly reduced in juveniles exposed to oil during embryonic development (P < 0.001; Fig. 2). For pink salmon, Ucrit was determined for three treatments (control, ΣPAH 15.4  μg/L and 45.4  μg/L exposures). Absolute Ucrit was greatest in control fish (44.1 ± 1.7 cm/sec) and lowest in fish from the ΣPAH 45.4  μg/L exposure (34.7 ± 1.5 cm/sec, Fig. 2A). Although there was a weakly positive correlation between fish length and Ucrit in juvenile pink salmon (r = 0.394; Fig. S5A), the slope of the linear regression was significant (P < 0.001). Fish from the high oil treatment were significantly shorter (P = 0.002) and lighter (P = 0.006) relative to controls (Supplementary Fig. S5B, C). Fish also grew during the month-long data collection window (Supplementary Fig. S5D; PANCOVA < 0.001). Although the slopes for the two oil treatments were equal (PANCOVA = 0.915), the controls were bigger on a given date (PANCOVA = 0.001). However, dose-dependent reduction in swimming speed was not entirely explained by differences in fish size, in particular because the smaller oil-exposed fish had lower relative Ucrit. Critical swimming speed normalized by length (relative Ucrit) produced the same dose-dependent pattern and significance (Fig. 2B), and relative Ucrit in the ΣPAH 45.4  μg/L treatment group (4.6 ± 0.2 BL/sec) was significantly less than in controls (5.5 ± 0.2 BL/sec, P = 0.02). Reduction in relative Ucrit was also significant after accounting for time and growth using 2-factor ANOVA models that included either length and Ucrit or time and Ucrit.


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)

Embryonic oil exposure reduced critical swimming speed and maximum metabolic rate of juveniles.Mean Ucrit (±s.e.m.) is given as an absolute speed (A and C, cm/s) or relative to body length (B and D, BL/s) for (A,B) salmon exposed to clean effluent (ΣPAH 0.2  μg/L, N = 51) or oiled gravel effluent with ΣPAH 15  μg/L (N = 45) and 45  μg/L (N = 52); and (C,D) herring exposed to clean gravel effluent (ΣPAH 0.04  μg/L, N = 32) and oiled gravel effluent with ΣPAH 0.23  μg/L (N = 33). (E) Maximum metabolic rate (MMR) for juvenile herring during Ucrit assays. Oxygen consumption data passing statistical criteria (clean gravel, N = 23; oiled gravel, N = 22) were used to calculate MMR as described under Methods. For salmon data, P values are shown for effect of oil exposure from ANOVA while P values over oil-exposed groups represent comparison to controls in post-hoc analysis. For herring data, P values shown are for effect of treatment (oil exposure) and tank effect, respectively, from a nested ANOVA (replicate nested under treatment).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f2: Embryonic oil exposure reduced critical swimming speed and maximum metabolic rate of juveniles.Mean Ucrit (±s.e.m.) is given as an absolute speed (A and C, cm/s) or relative to body length (B and D, BL/s) for (A,B) salmon exposed to clean effluent (ΣPAH 0.2  μg/L, N = 51) or oiled gravel effluent with ΣPAH 15  μg/L (N = 45) and 45  μg/L (N = 52); and (C,D) herring exposed to clean gravel effluent (ΣPAH 0.04  μg/L, N = 32) and oiled gravel effluent with ΣPAH 0.23  μg/L (N = 33). (E) Maximum metabolic rate (MMR) for juvenile herring during Ucrit assays. Oxygen consumption data passing statistical criteria (clean gravel, N = 23; oiled gravel, N = 22) were used to calculate MMR as described under Methods. For salmon data, P values are shown for effect of oil exposure from ANOVA while P values over oil-exposed groups represent comparison to controls in post-hoc analysis. For herring data, P values shown are for effect of treatment (oil exposure) and tank effect, respectively, from a nested ANOVA (replicate nested under treatment).
Mentions: We used critical swimming speed (Ucrit) as a measure of cardiorespiratory performance in juvenile pink salmon and Pacific herring. Ucrit is the maximum sustained swimming speed reached at the point of fatigue and at which maximum sustained oxygen uptake occurs22. A swim tunnel respirometer designed for small fish (4–12 g) was used to measure Ucrit for both species at 8–9° C following seven to eight months of growth in clean water. For both species, Ucrit was significantly reduced in juveniles exposed to oil during embryonic development (P < 0.001; Fig. 2). For pink salmon, Ucrit was determined for three treatments (control, ΣPAH 15.4  μg/L and 45.4  μg/L exposures). Absolute Ucrit was greatest in control fish (44.1 ± 1.7 cm/sec) and lowest in fish from the ΣPAH 45.4  μg/L exposure (34.7 ± 1.5 cm/sec, Fig. 2A). Although there was a weakly positive correlation between fish length and Ucrit in juvenile pink salmon (r = 0.394; Fig. S5A), the slope of the linear regression was significant (P < 0.001). Fish from the high oil treatment were significantly shorter (P = 0.002) and lighter (P = 0.006) relative to controls (Supplementary Fig. S5B, C). Fish also grew during the month-long data collection window (Supplementary Fig. S5D; PANCOVA < 0.001). Although the slopes for the two oil treatments were equal (PANCOVA = 0.915), the controls were bigger on a given date (PANCOVA = 0.001). However, dose-dependent reduction in swimming speed was not entirely explained by differences in fish size, in particular because the smaller oil-exposed fish had lower relative Ucrit. Critical swimming speed normalized by length (relative Ucrit) produced the same dose-dependent pattern and significance (Fig. 2B), and relative Ucrit in the ΣPAH 45.4  μg/L treatment group (4.6 ± 0.2 BL/sec) was significantly less than in controls (5.5 ± 0.2 BL/sec, P = 0.02). Reduction in relative Ucrit was also significant after accounting for time and growth using 2-factor ANOVA models that included either length and Ucrit or time and Ucrit.

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