Species-Specific Responses of Juvenile Rockfish to Elevated pCO2: From Behavior to Genomics

In the California Current ecosystem, global climate change is predicted to trigger large-scale changes in ocean chemistry within this century. Ocean acidification—which occurs when increased levels of atmospheric CO2 dissolve into the ocean—is one of the biggest potential threats to marine life. In a coastal upwelling system, we compared the effects of chronic exposure to low pH (elevated pCO2) at four treatment levels (i.e., pCO2 = ambient [500], moderate [750], high [1900], and extreme [2800 μatm]) on behavior, physiology, and patterns of gene expression in white muscle tissue of juvenile rockfish (genus Sebastes), integrating responses from the transcriptome to the whole organism level. Experiments were conducted simultaneously on two closely related species that both inhabit kelp forests, yet differ in early life history traits, to compare high-CO2 tolerance among species. Our findings indicate that these congeners express different sensitivities to elevated CO2 levels. Copper rockfish (S. caurinus) exhibited changes in behavioral lateralization, reduced critical swimming speed, depressed aerobic scope, changes in metabolic enzyme activity, and increases in the expression of transcription factors and regulatory genes at high pCO2 exposure. Blue rockfish (S. mystinus), in contrast, showed no significant changes in behavior, swimming physiology, or aerobic capacity, but did exhibit significant changes in the expression of muscle structural genes as a function of pCO2, indicating acclimatization potential. The capacity of long-lived, late to mature, commercially important fish to acclimatize and adapt to changing ocean chemistry over the next 50–100 years is likely dependent on species-specific physiological tolerances

Effects of elevated CO2 on growth rates of larval northern rock sole (Lepidopsetta polyxystra)

Keywords: CO2; fish larvae; northern rock sole; Lepidopsetta polyxystra; ocean acidification; life history; larval developmen

Effects of elevated CO₂ levels on eggs and larvae of a North Pacific flatfish

The Bering Sea and Gulf of Alaska support a number of commercially important flatfish fisheries. These high latitude ecosystems are predicted to be most immediately impacted by ongoing ocean acidification, but the range of responses by commercial fishery species has yet to be fully explored. In this study, we examined the growth responses of northern rock sole (Lepidopsetta polyxystra) eggs and larvae across a range of CO₂ levels (ambient to 1500 µatm) to evaluate the potential sensitivity to ocean acidification. Laboratory-spawned eggs and larvae were reared at 8°C in a flow-through culture system in which CO₂ levels were maintained via computer-controlled injection of CO₂ into a seawater conditioning tank. Overall, we observed only minor effects of elevated CO₂ level on sizes of northern rock sole larvae. Size at hatch differed among offspring from four different females, but there was no significant effect of CO₂ level on egg survival or size at hatch. In three separate larval growth trials, there was little effect of CO₂ level on growth rates through the first 28 d post-hatch (DPH). However, in the one trial extended to 60 DPH, fish reared at the highest CO₂ level had lower condition factors after 28 DPH, suggesting that larvae undergoing metamorphosis may be more sensitive to environmental hypercapnia than earlier pre-flexion stages. These results suggest that while early life stages of northern rock sole are less sensitive to ocean acidification than previously examined flatfish, they may be more sensitive to elevated CO₂ levels than a previously studied gadid with a similar geographic range.Keywords: hypercapnia, flatfish, growth rate, ocean acidification, climate change, early life histor

Species-Specific Responses of Juvenile Rockfish to Elevated pCO2: From Behavior to Genomics.

In the California Current ecosystem, global climate change is predicted to trigger large-scale changes in ocean chemistry within this century. Ocean acidification-which occurs when increased levels of atmospheric CO2 dissolve into the ocean-is one of the biggest potential threats to marine life. In a coastal upwelling system, we compared the effects of chronic exposure to low pH (elevated pCO2) at four treatment levels (i.e., pCO2 = ambient [500], moderate [750], high [1900], and extreme [2800 μatm]) on behavior, physiology, and patterns of gene expression in white muscle tissue of juvenile rockfish (genus Sebastes), integrating responses from the transcriptome to the whole organism level. Experiments were conducted simultaneously on two closely related species that both inhabit kelp forests, yet differ in early life history traits, to compare high-CO2 tolerance among species. Our findings indicate that these congeners express different sensitivities to elevated CO2 levels. Copper rockfish (S. caurinus) exhibited changes in behavioral lateralization, reduced critical swimming speed, depressed aerobic scope, changes in metabolic enzyme activity, and increases in the expression of transcription factors and regulatory genes at high pCO2 exposure. Blue rockfish (S. mystinus), in contrast, showed no significant changes in behavior, swimming physiology, or aerobic capacity, but did exhibit significant changes in the expression of muscle structural genes as a function of pCO2, indicating acclimatization potential. The capacity of long-lived, late to mature, commercially important fish to acclimatize and adapt to changing ocean chemistry over the next 50-100 years is likely dependent on species-specific physiological tolerances

Species-Specific Responses of Juvenile Rockfish to Elevated <i>p</i>CO₂: From Behavior to Genomics

<div><p>In the California Current ecosystem, global climate change is predicted to trigger large-scale changes in ocean chemistry within this century. Ocean acidification—which occurs when increased levels of atmospheric CO₂ dissolve into the ocean—is one of the biggest potential threats to marine life. In a coastal upwelling system, we compared the effects of chronic exposure to low pH (elevated <i>p</i>CO₂) at four treatment levels (i.e., <i>p</i>CO₂ = ambient [500], moderate [750], high [1900], and extreme [2800 μatm]) on behavior, physiology, and patterns of gene expression in white muscle tissue of juvenile rockfish (genus <i>Sebastes</i>), integrating responses from the transcriptome to the whole organism level. Experiments were conducted simultaneously on two closely related species that both inhabit kelp forests, yet differ in early life history traits, to compare high-CO₂ tolerance among species. Our findings indicate that these congeners express different sensitivities to elevated CO₂ levels. Copper rockfish (<i>S</i>. <i>caurinus</i>) exhibited changes in behavioral lateralization, reduced critical swimming speed, depressed aerobic scope, changes in metabolic enzyme activity, and increases in the expression of transcription factors and regulatory genes at high <i>p</i>CO₂ exposure. Blue rockfish (<i>S</i>. <i>mystinus</i>), in contrast, showed no significant changes in behavior, swimming physiology, or aerobic capacity, but did exhibit significant changes in the expression of muscle structural genes as a function of <i>p</i>CO₂, indicating acclimatization potential. The capacity of long-lived, late to mature, commercially important fish to acclimatize and adapt to changing ocean chemistry over the next 50–100 years is likely dependent on species-specific physiological tolerances.</p></div

Summary of the range of exposure duration, acclimation time, time per trial, recovery period, and sample size for copper and blue rockfish used to test behavioral and physiological responses to elevated <i>p</i>CO₂.

<p>Note: Individual fish were used successively in the different trials to enable tracking of performance measures. Data from fish that did not behave normally in a particular trial were excluded (e.g., refusal to swim in the U_crit test). In addition, 2 of 12 blue rockfish individuals that were sequenced had low quality reads and were subsequently excluded from the differential gene expression analysis.</p

Mean carbonate chemistry conditions (± standard error) in the experimental system.

<p>Shown are mean values of dissolved organic carbon (DIC), total alkalinity, pH (total scale), <i>p</i>CO₂, and temperature.</p

Enzyme activity ratios for lactate dehydrogenase and citrate synthase (LDH:CS) in white muscle tissue of (A) copper and (B) blue rockfish following chronic exposure to extreme <i>p</i>CO₂ (~2800 μatms) or control (~550 μatms) treatments.

<p>Copper rockfish exhibited a significant increase in aerobic enzyme activity relative to anaerobic activity (i.e., lower LDH:CS ratio) from the control to extreme high <i>p</i>CO₂ treatments (two-way ANOVA; Species×Treatment: <i>F</i>_{<i>1</i>,<i>24</i>} = 4.46, <i>P</i> = 0.045), whereas blue rockfish did not differ in LDH:CS activity among treatments.</p

Gene expression profiles (A) and Gene Ontology (GO) functional categories (B) for copper and blue rockfish muscle tissue as a function of <i>p</i>CO₂ treatment.

<p>(A) Heatmaps display significant differential gene expression (DE) for copper (<i>n</i> = 147) and blue (<i>n</i> = 358) rockfish (FDR<0.001) among <i>p</i>CO₂ treatments; green = up-regulation, red = down-regulation. Each column represents an individual fish (<i>n</i> = 15 copper rockfish and <i>n</i> = 10 blue rockfish). Genes are ordered by similarity in gene expression profile and differ in both order and identity between the two species (only 14 DE genes were in common between the two species). Hierarchical (Euclidean) clustering was used to group similar gene expression profiles, labeled along the right side of each heatmap and listed in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0169670#pone.0169670.s002" target="_blank">S2</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0169670#pone.0169670.s003" target="_blank">S3</a> Tables. (B) GO categories show relative differences between copper and blue rockfish in the percentage of annotated genes that were differentially expressed, as classified by GO molecular function or biological process. Broken out pie wedges highlight GO categories that were more expressed in one species than the other. Copper rockfish show significant up-regulation of genes involved in transcription and biological regulation at high <i>p</i>CO₂ and down-regulation at low <i>p</i>CO₂. In contrast, blue rockfish differentially express muscle structural genes across <i>p</i>CO₂ treatments.</p