Climatic regulation of the neurotoxin domoic acid

S. Morgaine McKibben, William Peterson, A. Michelle Wood, Vera L. Trainer, Matthew Hunter, and Angelicque E. White
PNAS January 10, 2017 114 (2) 239-244; published ahead of print January 9, 2017 https://doi.org/10.1073/pnas.1606798114

  1. Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved November 30, 2016 (received for review April 28, 2016)

Article Figures & SI

Figures

  • Fig. 1.
    Fig. 1.

    (A) Warm and cool ocean regimes, (B) local SST anomaly, and (C and D) biological response. (A) PDO (red or blue vertical bars) and ONI (black line) indices; strong (S) to moderate (M) El Niño (≥1) and La Niña (≤− 1) events are labeled. (B) SST anomaly 20 nm off central OR. (C) The CSR anomaly 5 nm off central OR. (D) Monthly OR coastal maximum DA levels in razor clams (vertical bars); horizontal black line is the 20-ppm closure threshold; data below 20 ppm are not shown. Black line in D shows the spring biological transition date (right y axis). (E) Black boxes indicate the duration of upwelling season each year; red vertical bars indicate the timing of annual DA maxima in relationship to upwelling. Gray shaded regions are warm regimes based on the PDO. Dashed vertical lines indicate onset of the six major DA events. The September 2014 arrival of the NE Pacific Warm Anomaly (colloquially termed “The Blob”) to the OR coastal region is labeled on B. “X” symbols along the x axes indicate that no data were available for that month (B–D).

  • Fig. S1.
    Fig. S1.

    Regressions of sum of the PDO and ONI for March (x axis) and five OR coast parameters: (A) average water temperature in the Yaquina estuary during winter, (B) March SST anomaly 20 nm offshore, (C) average alongshore currents for March–April (more negative means stronger southward flow), (D) the spring biological transition date, and (E) the annual maximum DA concentration in razor clams for the OR coast. Triangles indicate the five highest annual DA values on record. The year 2002 is marked on each plot; this year saw the fifth highest DA on record but is associated with cooler ocean conditions than predicted by these plots. Statistical results are given in Table S2.

  • Fig. 2.
    Fig. 2.

    DA risk analysis model output (yellow to red) and DA levels in OR and WA razor clams (vertical bars) from 1992–2015. Model values indicate increased risk of elevated DA based on proxies of warm ocean parameters; model values are only calculated during upwelling season, when concentrations of phytoplankton are likely to be greatest each year. White regions indicate that elevated DA is least likely, as the model equals zero and/or it is downwelling season. From top to bottom, monthly maximum DA values (vertical bars) are latitudinally binned as follows: WA (46.3°N to 48°N), northern OR (45°N to 46.3°N), central OR (44°N to 45°N), and southern OR (42°N to 44°N). Bar length is proportional to the monthly maximum DA value. Color indicates DA ≥ 20 ppm (black lines), from 1 to <20 ppm (gray lines), or not detected (gray squares). An absence of points indicates no DA data available. Annual DA maxima used in model evaluation are highlighted with yellow squares. Results of model evaluation are shown in Tables S3 and S4. See Fig. S2 for CA risk analysis.

  • Fig. S2.
    Fig. S2.

    DA risk analysis model output (yellow to red) and DA levels in CA shellfish (vertical bars) from 2000–2015. Model values indicate increased risk of elevated DA based on proxies of warm ocean parameters; model values are only calculated during upwelling season, when concentrations of phytoplankton are likely to be greatest each year. White regions indicate that elevated DA is least likely (the model equals zero and/or it is downwelling season). From top to bottom, monthly maximum DA values (vertical bars) are latitudinally binned as follows: northern CA (39°N to 42°N), central CA (36°N to 39°N), southern CA (34°N to 36°N), and far southern CA (32°N to 34°N). Bar length is proportional to the monthly maximum DA value. Color indicates DA ≥ 20 ppm (black lines), between 1 ppm and <20 ppm (gray lines), or not detected (gray squares). An absence of points indicates that no DA data were available. Annual DA maxima used in model evaluation are highlighted with yellow squares. Results of model evaluation are shown in Tables S3 and S4. When comparing to Fig. 2, risk analysis for OR and WA, note the shorter x axis here. Also, CA DA levels are concentrations from predominantly mussels. Sampling periods also differ from OR and WA: In CA, samples are event-based, i.e., taken only when blooms of Pseudo-nitzschia are observed.

Tables

  • Table S1.

    Cross-correlation results for monthly time series and PDO and ONI

    Variablesr, moLag range (range of r values), monDescription
    x = PDO
     y = ONI0.59− 4 to +3231ONI typically lags PDO by 0 mo, with a range of − 4 mo to +3 mo
    (0)(0.52 to 0.59)
     y = SST anomaly0.54− 1 to +1231SST anomaly typically lags PDO by 0 mo, with a range of − 1 mo to +1 mo
    (0)(0.45 to 0.54)
     y = CSR anomaly0.480 to +9231CSR typically lags PDO by 4 mo, with a range of 0 mo to 9 mo
    (+4)(0.39 to 0.48)
     y = monthly maximum DA0.38+2 to +10231DA typically lags PDO by 6 mo, with a range of 2 mo to 10 mo
    (+6)(0.28 to 0.38)
    x = ONI
     y = SST anomaly0.39− 3 to +5231SST anomaly typically lags ONI by 0 mo, with a range of − 3 mo to +5 mo
    (0)(0.30 to 0.39)
     y = CSR anomaly0.54+3 to +8231CSR typically lags ONI by 6 mo, with a range of 3 mo to 8 mo
    (6)(0.45 to 0.54)
     y = monthly maximum DA0.45+7 to +14231DA typically lags ONI by 9 mo, with a range of 7 mo to 14 mo
    (9)(0.35 to 0.45)

    • Column 1 shows the maximum correlation value (rmax), where r is the cross-correlation value, and the corresponding lag in months (in parentheses). Variables were also significantly related across a range of r; this range (column 2) spans rmax to rmax −1, and the associated lag is in parentheses. Column 3 shows the n values of the time series, where n is the number of values in cross-correlation analysis. Column 4 gives a brief description of the results shown in each row.

  • Table S2.

    Annual linear regression results for March PDO and ONI values (x values, columns) versus physical and biological parameters (y values, rows) reported as r squared values with the corresponding significance level in parentheses

    Dependent variablesSummed March PDO + ONIMarch PDOMarch ONIMaximum annual DA, ppm
    Mean Yaquina Estuary water temperature, December–March (n = 17), °C0.810.690.630.68
    (P<0.0001)(P< 0.0001)(P< 0.0001)(P< 0.0001)
    SST anomaly, March (n = 20), °C0.660.670.370.27
    (P< 0.0001)(P< 0.0001)(P = 0.0047)(P = 0.0196)
    CSR anomaly, March (n = 19)0.510.430.420.23
    (P = 0.0006)(P = 0.0022)(P = 0.0025)(P = 0.0379)
    Mean alongshore currents, March–April (n = 15), cm s−10.220.290.0700.22
    (P = 0.0771)(P = 0.0376)(P = 0.3422)(P = 0.0758)
    Annual spring biological transition day (n = 20), year–day0.700.650.470.53
    (P< 0.0001)(P< 0.0001)(P = 0.0009)(P = 0.0003)
    Maximum annual DA in razor clams (n = 20), ppm0.630.500.54n/a
    (P< 0.0001)(P = 0.0005)(P = 0.0002)

    • All y values were measured near the central OR coast, except for DA values in razor clams, which were measured coastwide. Bold values are significant at a 95% confidence interval or better.

  • Table S3.

    Evaluative metrics of DA risk model performance

    NorthernCentralSouthernNorthernCentralSouth/centralSouthern
    Evaluative metricsWAORORORCACACACA
    Actual number of DA maxima captured*1088856610
    Expected number of DA maxima†1919202012131313
    Number expected during undersampled years‡038107352
    Adjusted number of expected events§19161210510811
    Approximate number of false positives98420421
    Percent false positives#47503330040259
    DA maxima occurring during a month with elevated risk, i.e., warm, upwelling-favorable conditions635445NaNNaN
    DA maxima occurring during the 1 mo following upwelling season121310NaNNaN
    Total number of upwelling-associated annual DA maxima∥756755NaNNaN
    Percent of DA maxima during warm upwelling season conditions**3731507010050NaNNaN
    Total number of months with a sample2912311459857129129142
    Total number possible months300300300300192192192192

    • Rows 1 to 6 report calculations for estimates of false positives for each bin of DA data. Rows 7 to 10 report calculations for the percentage of annual maxima that coincided with upwelling season. Upwelling-related values for south and south central CA were not calculated due to the nearly year-round upwelling season that occurs there.

    • ↵* Number of annual DA maxima values exceeding 20 ppm in bin.

    • ↵† Positive risk values for ≥3 consecutive months at any latitude in bin.

    • ↵‡ Number of expected years that were undersampled, i.e., had less than 6 mo with at least one DA sample in the bin.

    • ↵§ Number of expected years minus undersampled years.

    • ↵ Actual minus expected minus undersampled years.

    • ↵# Number of false positives divided by adjusted number of expected years × 100.

    • ↵∥ Sum of the number of annual DA maxima that occurred during elevated risk (i.e., upwelling-favorable conditions) and those that occurred 1 mo after upwelling season terminated, i.e., during the annual transition from upwelling to downwelling-favorable conditions.

    • ↵** Sum of the total number of upwelling associated maxima divided by adjusted number of expected years × 100.

  • Table S4.

    Linear regression results between annual metrics of DA events (y values, rows) and log10 (annual maximum DA values) (x value)

    x = log10(annual DA maximum)
    Independent variablesStates includedr2 (P value)N
    y1 = Model value coincident with annual maximumWA & OR0.38 (P < 0.0053)19
    CA0.26 (P < 0.012)23
    WA, OR, & CA0.28 (P < 0.00027)42
    y2 = Annual maximum value of risk modelWA & OR0.30 (P < 0.0023)28
    CA0.35 (P < 0.0018)25
    WA, OR, & CA0.28 (P < 0.000011)53
    y3 = March PDO + ONIWA & OR0.31 (P < 0.0013)30
    CA0.33 (P < 0.0029)25
    WA, OR & CA0.27 (P < 0.000042)55

    • Data reported by state groupings (column 2) according to r2 and P values (column 3) and number of data points (column 4). All values are significant at a 99% confidence interval or better.

Data supplements

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Climatic regulation of the neurotoxin domoic acid
S. Morgaine McKibben, William Peterson, A. Michelle Wood, Vera L. Trainer, Matthew Hunter, Angelicque E. White
Proceedings of the National Academy of Sciences Jan 2017, 114 (2) 239-244; DOI: 10.1073/pnas.1606798114
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