Research ArticleOCEANOGRAPHY

Thermal stress reduces pocilloporid coral resilience to ocean acidification by impairing control over calcifying fluid chemistry

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Science Advances  08 Jan 2021:
Vol. 7, no. 2, eaba9958
DOI: 10.1126/sciadv.aba9958
  • Fig. 1 Calcifying fluid pHcf-based boron isotopes.

    Panels show measured parameters as a function of treatment pHsw. Blue squares correspond to 28°C, red triangles correspond to 31°C, solid symbols represent treatment averages, and open symbols represent data for individual coral specimens. (A) and (B) show net calcification rate as percent change in skeletal mass throughout the experiment (7). (C) and (D) show δ11B measured for P. damicornis and S. pistillata, respectively, and independent measurements of δ11B of S. pistillata by Alfred Wegener Institute for Polar and Marine Research (AWI), with individuals shown in open dark gray and treatment averages shown in solid gray. Dotted horizontal lines represent zero calcification. (E) and (F) show calculated pHcf (see the main text) for P. damicornis and S. pistillata, respectively. Best-fit model (linear or nonlinear regressions) was determined using GraphPad based on lowest akaike information criteria (AIC); solid lines indicate significant regressions. Dashed gray lines represent 1:1 ratio of pHcf:pHsw for comparison to observed trends (28°C, dark; 31°C, light). Error bars are given in SEM and envelopes for the regressions represent 95% confidence interval.

  • Fig. 2 Carbonate chemistry of the calcifying fluid–based boron proxies.

    Panels show measured parameters as a function of treatment pHsw. Blue squares correspond to 28°C, red triangles correspond to 31°C, solid symbols represent treatment averages, and open symbols represent data for individual coral specimens. (A) and (B) show net calcification rate as percent change in skeletal mass throughout the experiment (7). (C) and (D) show recalculated [CO32−]cf. (E) and (F) show calculated DICcf. (G) and (H) show calculated saturation state of aragonite in the calcifying fluid (Ωcf). Gray rectangles in (D), (F), and (H) represent the range (2 SD) of LIX data (32) for S. pistillata [pH 7.94 (total scale), T = 25°C, S = 38]. Best-fit model (linear or nonlinear regressions) was determined using GraphPad based on lowest AIC. Solid lines indicate significant regressions (P < 0.05). Dashed gray lines represent 1:1 ratio of [CO32−]cf:[CO32−]sw, DICcf:DICsw, or Ωcfsw for comparison to observed trends (28°C, dark; 31°C, light). Error bars are given in SEM and envelopes for the regressions represent 95% confidence interval.

  • Fig. 3 Effect of temperature on the carbonate chemistry of the calcifying fluid in this study.

    Effect of temperature on pHcf_δ11B (A) and DICcf (B) of S. pistillata (green) and P. damicornis (orange). Error bars are given as SEM.

  • Fig. 4 Compilation of pHcf under OA from direct and indirect measurements for S. pistillata and P. damicornis.

    Compilation of existing pHcf data from microelectrode, pH-sensitive-dye (SNARF), and boron isotope data. (A) S. pistillata. (B) P. damicornis. Error bars are given in SD.

  • Fig. 5 Comparison between pHcf from skeletal δ11B and direct LIX measurements.

    Comparison of pHcf from skeletal δ11B (pHcf_δ11B) and pHcf from microelectrode measurements (7) in the light (pHcf_light, black dots) and in the dark (pHcf_dark, gray triangles) for individual coral specimens of P. damicornis (A) and for S. pistillata (B) measured in the same samples. LRs of pHcf_light (dashed black line), pHcf_dark (dashed gray line), and both pHcf-based microelectrode (orange line) versus pHcf_δ11B. The black line represents 1:1 ratio of pHcf_δ11B:pHcf_microelectrode for comparison to observed trends. The orange line is the LR between pHcf from δ11B and pHcf derived from microelectrode (both light and dark), and the orange envelop represents the 95% confidence interval for LR.

  • Fig. 6 pHcf and DICcf from boron proxies and pHcf from LIX measurements.

    (A to C) Comparison between averages of boron-based pHcf (blue or red symbols) and microelectrode-derived pHcf in the light (open symbols) and in the dark (solid gray symbols) at the two temperature treatments for P. damicornis [(A) 28°C; no microelectrode pHcf data at 31°C] and S. pistillata [(B) 28°C and (C) 31°C]. LRs of pHcf_light (orange, 28°C; green, 31°C), pHcf_dark (black, 28°C; gray, 31°C), and pHcf_δ11B (blue, 28°C; red, 31°C) versus pH treatment. (D to F) DICcf data calculated from B/Ca and δ11B-derived pHcf for P. damicornis [(D) 28°C; no microelectrode pH data at 31°C] and S. pistillata [(E) 28°C and (F) 31°C]. Dashed gray lines represent 1:1 ratio of pHcf:pHsw for comparison to observed trends (28°C, dark; 31°C, light). Error bars are given in SEM and envelopes for the regressions represent 95% confidence interval.

  • Table 1 Measured and calculated seawater parameters (±SE) from the culturing experiments (S, salinity; T, temperature; pH (NBS scale); DIC, dissolved inorganic carbon; Alkalinity, total alkalinity; pH on total scale; [CO32−], carbonate ion; [HCO3], bicarbonate ion; [CO2], partial pressure of CO2; ΩA, saturation state of seawater with respect to aragonite).

    ExperimentSeawater measured parameters
    δ11Bsw*
    (‰)
    S
    (psu)
    T
    (°C)
    pH
    (NBS scale)
    DIC
    (μmol/kg-seawater)
    Alkalinity
    (μmol/kg-seawater)
    Exp1 (400 ppm, 28°C)41.02 ± 0.4934.9 ± 0.128.29 ± 0.018.27 ± 0.012480 ± 402915 ± 49
    Exp2 (400 ppm, 31°C)40.17 ± 0.3335.6 ± 0.131.72 ± 0.068.24 ± 0.012350 ± 442774 ± 54
    Exp3 (1000 ppm, 28°C)41.36 ± 0.1335.4 ± 0.127.88 ± 0.028.04 ± 0.012645 ± 442939 ± 46
    Exp4 (1000 ppm, 31°C)41.93 ± 0.2036.0 ± 0.130.83 ± 0.028.12 ± 0.012755 ± 373083 ± 40
    Exp5 (2800 ppm, 28°C)40.97 ± 0.1535.8 ± 0.128.17 ± 0.027.62 ± 0.012861 ± 822907 ± 81
    Exp6 (2800 ppm, 31°C)41.35 ± 0.1235.7 ± 0.130.93 ± 0.027.69 ± 0.013223 ± 573290 ± 56
    ExperimentSeawater calculated parameters
    pCO2
    (ppmv)
    pH**
    (total scale)
    [CO32−]
    (μmol/kg-seawater)
    [HCO3]
    (μmol/kg-seawater)
    [CO2]
    (μmol/kg-seawater)
    ΩA
    Exp1 (400 ppm, 28°C)466 ± 88.14 ± 0.01334 ± 92133 ± 3312.3 ± 0.25.38 ± 0.14
    Exp2 (400 ppm, 31°C)499 ± 98.09 ± 0.01320 ± 112017 ± 3612.3 ± 0.35.20 ± 0.18
    Exp3 (1000 ppm, 28°C)925 ± 157.90 ± 0.01217 ± 62424 ± 3524.6 ± 0.43.48 ± 0.10
    Exp4 (1000 ppm, 31°C)885 ± 127.97 ± 0.01265 ± 42468 ± 3522.0 ± 0.44.28 ± 0.07
    Exp5 (2800 ppm, 28°C)2807 ± 1207.49 ± 0.0190 ± 32697 ± 7774.3 ± 3.21.44 ± 0.04
    Exp6 (2800 ppm, 31°C)3194 ± 1367.55 ± 0.01113 ± 43030 ± 5479.5 ± 3.41.83 ± 0.06

    11Bsw-based average of δ11Bsw1 and δ11Bsw2 (see table S5) for each condition.

    **pH on total scale recalculated on the basis of pH measured on NBS scale during experiment.

    • Table 2 Measured values of δ11B and elemental ratios (B/Ca) within the skeletons of P. damicornis and corresponding reconstructed parameters of the calcifying fluid (pHcf, [CO32−]cf, and DICcf).

      Measured values of δ11B and elemental ratios (B/Ca) within the skeletons of P. damicornis and corresponding reconstructed parameters of the calcifying fluid (pHcf, [CO32−]cf, and DICcf)..

      Culture conditionsAnalytical resultsCalculated parameters
      pCO2swTpHswTankδ11Bc1 (±2 SD)δ11Bc2 (±2 SD)δ11Baverage (±2 SD)B/Ca (±2 SD)pHcf[CO32−]cf (±1 SE)DICcf (±1 SE)
      (ppm)(°C)(total scale)(‰)(‰)(‰)(μmol/mol)(total scale)(μmol/kg)(μmol/kg)
      Pocillopora damicornis
      466288.14119.70 ± 0.1019.65 ± 0.1019.68 ± 0.07472 ± 118.04522 ± 664458 ± 199
      466288.14221.52 ± 0.1021.63 ± 0.1021.58 ± 0.07545 ± 118.19621 ± 573891 ± 162
      466288.14322.76 ± 0.1022.65 ± 0.1022.71 ± 0.07449 ± 118.28877 ± 704694 ± 206
      466288.14423.67 ± 0.1123.68 ± 0.1123.68 ± 0.08492 ± 118.34894 ± 654240 ± 175
      466288.14124.42 ± 0.3924.42 ± 0.39489 ± 118.39975 ± 764231 ± 178
      466288.14219.01 ± 0.3919.01 ± 0.39460 ± 117.97463 ± 814513 ± 222
      499318.09422.02 ± 0.2122.09 ± 0.2122.06 ± 0.29537 ± 118.25759 ± 613840 ± 157
      499318.09422.38 ± 0.0922.38 ± 0.09537 ± 118.27789 ± 553834 ± 162
      499318.09121.02 ± 0.0921.02 ± 0.09501 ± 118.17707 ± 574130 ± 176
      499318.0922.01 ± 0.1122.02 ± 0.1122.01 ± 0.08500 ± 118.24809 ± 574126 ± 174
      499318.09318.53 ± 0.1118.50 ± 0.1118.51 ± 0.08504 ± 117.96455 ± 584000 ± 188
      499318.09415.56 ± 0.1115.53 ± 0.1115.55 ± 0.08470 ± 117.60184 ± 603459 ± 461
      925287.90217.22 ± 0.1117.23 ± 0.1117.23 ± 0.08435 ± 117.73263 ± 584329 ± 339
      925287.90119.78 ± 0.1119.63 ± 0.1119.71 ± 0.08558 ± 118.01422 ± 453807 ± 162
      925287.90322.98 ± 0.2622.82 ± 0.2622.90 ± 0.18492 ± 118.27800 ± 554361 ± 178
      925287.90222.25 ± 0.0922.25 ± 0.09491 ± 118.22735 ± 544383 ± 185
      925287.90421.60 ± 0.0921.60 ± 0.09503 ± 118.17652 ± 544280 ± 178
      925287.90121.69 ± 0.0921.69 ± 0.09619 ± 118.18538 ± 423482 ± 136
      885317.97421.32 ± 0.0921.32 ± 0.09743 ± 118.07387 ± 382812 ± 114
      885317.97318.94 ± 0.0918.94 ± 0.09474 ± 117.84356 ± 564141 ± 230
      885317.97121.89 ± 0.2121.85 ± 0.2121.87 ± 0.158.11
      885317.97321.88 ± 0.0921.88 ± 0.09592 ± 118.11533 ± 463550 ± 146
      885317.97317.84 ± 0.1117.80 ± 0.1117.82 ± 0.08524 ± 117.70217 ± 503422 ± 286
      885317.97121.47 ± 0.1121.46 ± 0.1121.46 ± 0.08441 ± 118.08668 ± 614751 ± 208
      2807287.49122.59 ± 0.2622.53 ± 0.2622.56 ± 0.18460 ± 118.27865 ± 604673 ± 192
      2807287.49422.60 ± 0.1122.35 ± 0.1122.48 ± 0.08466 ± 118.26845 ± 574613 ± 187
      2807287.49321.19 ± 0.1121.24 ± 0.1121.21 ± 0.08422 ± 118.17782 ± 645118 ± 224
      2807287.49222.69 ± 0.1122.57 ± 0.1122.63 ± 0.08496 ± 118.27811 ± 544339 ± 175
      2807287.49221.48 ± 0.2121.48 ± 0.218.19
      3194317.55422.17 ± 0.3922.17 ± 0.39485 ± 118.18734 ± 694300 ± 178
      3194317.55220.47 ± 0.0920.47 ± 0.09486 ± 118.04557 ± 534266 ± 184
      3194317.55315.61 ± 0.0915.61 ± 0.09538 ± 117.3974 ± 7x2276 ± 108
      3194317.55416.06 ± 0.0916.06 ± 0.09518 ± 117.49113 ± 462774 ± 94
      3194317.55114.60 ± 0.1114.59 ± 0.1114.60 ± 0.08449 ± 117.0214 ± 4x950 ± 175
      3194317.55420.24 ± 0.1120.29 ± 0.1120.26 ± 0.08509 ± 118.02512 ± 504061 ± 180
      3194317.55214.00 ± 0.1113.94 ± 0.1113.97 ± 0.08523 ± 116.38

      pCO2sw, seawater pCO2 of the culture treatment.

      T, seawater temperature of the culture treatment.

      pHsw, seawater pH of the culture treatment.

      Tank, tank number where the sample was cultured.

      δ11Bc1, first measurement of the boron isotopic composition of the sample, uncertainty determined on reproducibility of the AE121 standard (2 SD).

      δ11Bc2, duplicate analysis of the boron isotopic composition of the sample, uncertainty determined on reproducibility of the AE121 standard (2 SD).

      δ11Baverage, average of δ11Bc1 and δ11Bc2 or δ11Bc1 if only one measurement was performed. When two measurements were carried out, uncertainty was calculated based on uncertainties of δ11Bc1 and δ11Bc2a = √ (Σiai)2)).

      B/Ca measured for the sample. Uncertainty is calculated as 2 SD of repeated measurements of the CamWuellestorfi standard (table S4).

      pHcf calculated from δ11B using (8) based on Monte Carlo simulation.

      [CO32−]cf calculated from B/Ca using (8).

      DICcf calculated from δ11B and B/Ca using (8).

      Uncertainties for [CO32−]cf and DICcf calculated using (8), Δ (1 SE) = √ (Σi(Δsysi+Δnonsysi)2), xuncertainty = Δnonsys (1 SE).Additional data not used in this study (Li/Ca, Mg/Ca and Sr/Ca) are presented in table S7 in the Supplementary Materials.

      • Table 3 Measured values of δ11B and elemental ratios (B/Ca) within the skeletons of S. pistillata and corresponding reconstructed parameters of the calcifying fluid (pHcf, [CO32−]cf, and DICcf).

        Measured values of δ11B and elemental ratios (B/Ca) within the skeletons of S. pistillata and corresponding reconstructed parameters of the calcifying fluid (pHcf, [CO32−]cf, and DICcf)..

        Culture conditionsAnalytical results
        pCO2swTpHswTankδ11Bc1 (±2 SD)δ11Bc2 (±2 SD)δ11Baverage (±2 SD)B/Ca (±2 SD)pHcf[CO32−]cf (±1 SE)DICcf (±1 SE)
        (ppm)(°C)(total scale)(‰)(‰)(‰)(μmol/mol)(total scale)(μmol/kg)(μmol/kg)
        Stylophora pistillata
        466288.14223.20 ± 0.3023.21 ± 0.3023.20 ± 0.21470 ± 118.31888 ± 704464 ± 191
        466288.142455 ± 11918 ± 714614 ± 194
        466288.142459 ± 11909 ± 704584 ± 190
        466288.14421.85 ± 0.3021.63 ± 0.3021.74 ± 0.21527 ± 118.21659 ± 624021 ± 166
        466288.14123.95 ± 0.2623.95 ± 0.26432 ± 118.361050 ± 784815 ± 216
        466288.14224.94 ± 0.2624.94 ± 0.26480 ± 118.431048 ± 704291 ± 181
        499318.09218.09 ± 0.2618.09 ± 0.26378 ± 117.92553 ± 845283 ± 284
        499318.09421.62 ± 0.0921.62 ± 0.09536 ± 118.21718 ± 543850 ± 163
        499318.09123.48 ± 0.0923.48 ± 0.09513 ± 118.34934 ± 593968 ± 163
        499318.091526 ± 11983 ± 634179 ± 184
        499318.09420.93 ± 0.2620.93 ± 0.26411 ± 118.16851 ± 795046 ± 231
        499318.09319.62 ± 0.0919.62 ± 0.09462 ± 118.06616 ± 634451 ± 203
        499318.09122.04 ± 0.0922.04 ± 0.09557 ± 118.24728 ± 533692 ± 160
        499318.091473 ± 11859 ± 624351 ± 187
        925287.90223.26 ± 0.3623.26 ± 0.36419 ± 118.29980 ± 775097 ± 217
        925287.90422.70 ± 0.2622.70 ± 0.26440 ± 118.25870 ± 674885 ± 207
        925287.90122.25 ± 0.2622.25 ± 0.26451 ± 118.22800 ± 644770 ± 204
        925287.90323.63 ± 0.2623.63 ± 0.26449 ± 118.32958 ± 674747 ± 200
        925287.90223.32 ± 0.2623.32 ± 0.26485 ± 118.30855 ± 624403 ± 184
        885317.97323.01 ± 0.2122.79 ± 0.2122.90 ± 0.158.19
        885317.97123.21 ± 0.3923.21 ± 0.39417 ± 118.21920 ± 825038 ± 220
        885317.97319.64 ± 0.2619.64 ± 0.26378 ± 117.91541 ± 795346 ± 286
        885317.97419.76 ± 0.2619.76 ± 0.26595 ± 117.92353 ± 503408 ± 161
        885317.97117.49 ± 0.2617.49 ± 0.26394 ± 117.65251 ± 734347 ± 474
        885317.97223.27 ± 0.3923.27 ± 0.39417 ± 118.22929 ± 845036 ± 219
        2807287.49322.11 ± 0.3922.11 ± 0.39384 ± 118.23983 ± 865622 ± 251
        2807287.49321.90 ± 0.3921.90 ± 0.39377 ± 118.22968 ± 865726 ± 257
        2807287.49421.51 ± 0.3921.51 ± 0.39357 ± 118.19969 ± 946046 ± 287
        2807287.49421.40 ± 0.3921.40 ± 0.39355 ± 118.18958 ± 956095 ± 286
        3194317.55421.74 ± 0.3921.74 ± 0.39410 ± 118.15819 ± 815101 ± 231
        3194317.55222.75 ± 0.3922.75 ± 0.39425 ± 118.22903 ± 794895 ± 214
        3194317.55322.62 ± 0.3622.62 ± 0.36408 ± 118.21928 ± 785106 ± 226
        3194317.55322.05 ± 0.3622.05 ± 0.36419 ± 118.17836 ± 784984 ± 218
        3194317.55119.15 ± 0.3919.15 ± 0.39342 ± 117.92605 ± 935888 ± 330
        3194317.55222.07 ± 0.2822.14 ± 0.2822.10 ± 0.20455 ± 118.17773 ± 614585 ± 202

        pCO2sw, seawater pCO2 of the culture treatment.

        T, seawater temperature of the culture treatment.

        pHsw, seawater pH of the culture treatment.

        Tank, tank number where the sample was cultured.

        δ11Bc1, first measurement of the boron isotopic composition of the sample, uncertainty determined on reproducibility of the AE121 standard (2 SD).

        δ11Bc2, duplicate analysis of the boron isotopic composition of the sample, uncertainty determined on reproducibility of the AE121 standard (2 SD).

        δ11Baverage, average of δ11Bc1 and δ11Bc2 or δ11Bc1 if only one measurement was performed. When two measurements were carried out uncertainty was calculated based on uncertainties of δ11Bc1: and δ11Bc2a = √ (Σiai)2)).

        B/Ca measured for the sample. Uncertainty is based 2 SD on the reproducibility of the CamWuellestorfi (table S4).

        pHcf calculated from δ11B using (8) based on Monte Carlo simulation.

        [CO32−]cf calculated from B/Ca using (8).

        DICcf calculated from δ11B and B/Ca using (8).

        Uncertainties for [CO32−]cf and DICcf calculated using (8), Δ (1 SE) = √ (Σi(Δsysi+Δnonsysi)2), xuncertainty = Δnonsys (1 SE).Additional data not used in this study (Li/Ca, Mg/Ca and Sr/Ca) are presented in table S7 in the Supplementary Materials.

        • Table 4 Measurements of pHcf from microelectrode in the light (pHcf_light) and dark (pHcf_dark), pHcf_δ11B calculated from skeletal δ11B, and estimated light:dark calcification ratios.

          pHcf_light (±SE)pHcf_dark (±SE)ΔpHlight-dark (±SE)pHcf_δ11B (±SE)Light:dark calcification
          (total scale)(total scale)(total scale)(total scale)
          P. damicornis
          pCO2 466 ppm, 28°C8.93 ± 0.308.03 ± 0.340.9 ± 0.58.20 ± 0.0719:81
          pCO2 925 ppm, 28°C8.43 ± 0.227.92 ± 0.220.5 ± 0.38.10 ± 0.0835:65
          pCO2 2807 ppm, 28°C8.24 ± 0.227.39 ± 0.170.9 ± 0.38.23 ± 0.0299:01
          S. pistillata
          pCO2 466 ppm, 28°C8.86 ± 0.077.80 ± 0.301.1 ± 0.68.29 ± 0.1250:50
          pCO2 925 ppm, 28°C8.53 ± 0.157.86 ± 0.280.6 ± 0.38.28 ± 0.0263:37
          pCO2 2807 ppm, 28°C8.20 ± 0.237.65 ± 0.140.6 ± 0.38.20 ± 0.01100:00*
          pCO2 499 ppm, 31°C8.71 ± 0.127.96 ± 0.240.9 ± 0.38.16 ± 0.0527:73
          pCO2 885 ppm, 31°C8.03 ± 0.146.95 ± 0.230.9 ± 0.38.04 ± 0.1099:01
          pCO2 3194 ppm, 31°C8.01 ± 0.097.06 ± 0.080.9 ± 0.18.14 ± 0.11100:00*

          pHcf_light, pHcf measured from microelectrode when the coral was in the light; uncertainty is reported as 1 SE of the replicates.

          pHcf_dark, pHcf measured from microelectrode when the coral was in the dark; uncertainty is reported as 1 SE of the replicates.

          ΔpHlight-dark, difference in light and dark pHcf microelectrode measurements pHcf_diurnal: pHcf calculated from δ11B; uncertainty is reported as 1 SE of the replicates.

          Light:dark calcification, light:dark calcification ratios obtained from the weighting of pHcf_light and pHcf_dark measurements required to generate the δ11B-based estimates of pHcf (pHcf_δ11B) calculated from average of measured specimens within a treatment.

          *When pHcf_diurnal average was > or = pHcf_light but still within errors of each other, we attributed a light:dark calcification of 100:00.

          Supplementary Materials

          • Supplementary Materials

            Thermal stress reduces pocilloporid coral resilience to ocean acidification by impairing control over calcifying fluid chemistry

            Maxence Guillermic, Louise P. Cameron, Ilian De Corte, Sambuddha Misra, Jelle Bijma, Dirk de Beer, Claire E. Reymond, Hildegard Westphal, Justin B. Ries, Robert A. Eagle

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