Research ArticleECOLOGY

Naturally acidified habitat selects for ocean acidification–tolerant mussels

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Science Advances  26 Apr 2017:
Vol. 3, no. 4, e1602411
DOI: 10.1126/sciadv.1602411
  • Fig. 1 Habitat carbonate system variability and juvenile settlement.

    (A) Averaged monthly pH values recorded from 2009 to 2011 in the habitats of the two tested populations. The inset depicts the location of the two habitats in North Sea and Baltic Sea (S, Sylt; K, Kiel; DK, Denmark; Ger, Germany). (B) Continuously measured seawater Pco2 in summer 2012 in Kiel Fjord. (C) Mussel larval settlement intensity on panels between July and September. The arrows correspond to the estimated planktonic phases of larvae settled in July, August, and September. Values are means ± SD.

  • Fig. 2 Larval performance of Baltic Sea and North Sea populations exposed to elevated Pco2.

    (A) PD I length of both populations declined at high Pco2, but Baltic larval size was less affected (n = 22 to 73). (B) Daily shell growth was similar for both populations and Pco2 treatments [no data (ND) for North Sea larvae at high Pco2 due to low survival on days 14 and 21]. (C) Survival rapidly declined in North Sea larvae exposed to elevated Pco2, whereas Baltic Sea larvae were less affected by elevated Pco2 from day 7 forward. Values are means ± SD; numbers in bracket state the number of measured individuals per Pco2 treatment.

  • Fig. 3 Flow chart of the experimental approach.

    (A) Collection of mussels from North Sea and Baltic Sea population, acclimation to North Sea conditions from December 2013 to April 2014, and subsequent transfer, spawning, and exposure to two Pco2 treatments. (B) Crossing schemes for F1 and F2 generation. In 2012, F0 animals (eight dams and eight sires) were crossed pairwise to generate 16 full-sib F1 families nested within four half-sib groups. Settled mussels were subsequently acclimated for 1 and 2 years. In 2013, F2 was generated by performing single-specimen crosses using pure F1 tolerant lines as well as tolerant and sensitive F1 families selected in, and long-term acclimated to, 390-, 1120-, and 2400-μatm (tolerant only) Pco2. In 2014, F2 was generated with three dams from four families of each line (tolerant from 390- and 2400-μatm Pco2 acclimation and sensitive from 390-μatm Pco2 acclimation only) crossed with one male from the tolerant family E6.

  • Fig. 4 Larval performance of F1 and F2 animals exposed to elevated Pco2.

    (A) PD I length declined with increasing Pco2 but remained larger in tolerant F1 families (n = 314 to 620) and (B) partly recovered in tolerant (T×T) but not sensitive (S×T) F2 offspring from high Pco2–treated parents (n = 902 to 1314). (C) Larval daily shell growth at elevated Pco2 was not affected in F1 offspring (D) but decreased in F2 larvae and further deteriorated with high-CO2 exposure of parental animals. (E) Larval survival decreased at high Pco2 but was higher in tolerant families compared to sensitive F1 families. (F) Parental selection and long-term acclimation at high Pco2 did not improve survival in the F2 generation. Values are means ± SD; numbers in brackets state the number of measured individuals per Pco2 treatment.

  • Table 1 Carbonate chemistry during the larval experiments and the long-term acclimation.

    Carbonate chemistry during the larval experiments and the long-term acclimation.. pH on total scale and CT were measured (n = 163), and AT, Pco2, [CO32−], and ΩAragonite were calculated using CO2SYS. NBS, National Bureau of Standards.

    Temperature (°C)Salinity (g kg−1)Pco2 treatment (μatm)CT (μmol kg−1)pH (total scale)Measured pH (NBS scale)AT (μmol kg−1)Pco2 (μatm)[CO32−] (μmol kg−1)ΩAragonite
    F1 larvae 201217.7 ± 0.115.5 ± 0.33901802 ± 467.97 ± 0.028.17 ± 0.071884 ± 51508 ± 1476.6 ± 4.91.23 ± 0.08
    11201889 ± 787.65 ± 0.017.75 ± 0.061897 ± 761128 ± 8238.6 ± 1.20.62 ± 0.02
    24001995 ± 507.39 ± 0.037.46 ± 0.051944 ± 512114 ± 10822.6 ± 1.40.36 ± 0.02
    F2 larvae 201317.1 ± 0.216.0 ± 0.43901916 ± 868.03 ± 0.208.16 ± 0.072026 ± 90476 ± 18199.8 ± 14.81.60 ± 0.24
    F2 larvae 201411202056 ± 547.64 ± 0.157.69 ± 0.012063 ± 871264 ± 16744.1 ± 33.50.71 ± 0.53
    24002078 ± 277.43 ± 0.157.43 ± 0.022032 ± 282093 ± 37928.7 ± 15.20.46 ± 0.24
    18.8 ± 0.116.0 ± 0.23901875 ± 128.05 ± 0.038.19 ± 0.031989 ± 17440 ± 2499.6 ± 5.31.62 ± 0.09
    Long-term acclimation (2012–2014)24002039 ± 257.40 ± 0.077.55 ± 0.071991 ± 132160 ± 35825.0 ± 4.30.41 ± 0.07
    11.4 ± 4.315.1 ± 2.13902044 ± 1257.84 ± 0.078.02 ± 0.062064 ± 122734 ± 10846.2 ± 12.10.71 ± 0.20
    11202108 ± 1187.57 ± 0.057.71 ± 0.072068 ± 1181381 ± 13625.7 ± 6.70.40 ± 0.11
    PC24002258 ± 2577.33 ± 0.067.44 ± 0.092146 ± 2532515 ± 38215.7 ± 4.60.24 ± 0.07
    15.5 ± 0.128.5 ± 0.23902160 ± 148.02 ± 0.028.16 ± 0.012334 ± 14462 ± 26136.0 ± 6.02.14 ± 0.09
    24002411 ± 307.33 ± 0.017.46 ± 0.012357 ± 292588 ± 4531.4 ± 0.60.49 ± 0.01

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/3/4/e1602411/DC1

    Supplementary Materials and Methods

    fig. S1. Geographic origin of the two tested populations from Kiel Fjord in the Baltic Sea and the island of Sylt in the North Sea.

    fig. S2. Analysis of the Pco2 data from Fig. 1B on Pco2 levels experienced by larvae settling in July, August, and September in Kiel Fjord (54°19.8′N; 10°9.0′E).

    fig. S3. Picture of an M. edulis larva, with an approximate shell length of 120 μm, at the PD I stage 2 days after fertilization.

    fig. S4. Egg diameter and fecundity of F0 and F1 dams.

    fig. S5. F1 egg diameter and F2 larval performance in 2014.

    table S1. Statistical analyses of population experiment.

    table S2. Main effect contrasts from Bayesian GLMMs.

    table S3. Statistical analyses of the transgenerational experiment in 2014.

    References (4854)

  • Supplementary Materials

    This PDF file includes:

    • Supplementary Materials and Methods
    • fig. S1. Geographic origin of the two tested populations from Kiel Fjord in the Baltic Sea and the island of Sylt in the North Sea.
    • fig. S2. Analysis of the PCO2 data from Fig. 1B on PCO2 levels experienced by larvae settling in July, August, and September in Kiel Fjord (54°19.8′N; 10°9.0′E).
    • fig. S3. Picture of an M. edulis larva, with an approximate shell length of 120 μm, at the PD I stage 2 days after fertilization .
    • fig. S4. Egg diameter and fecundity of F0 and F1 dams.
    • fig. S5. F1 egg diameter and F2 larval performance in 2014.
    • table S1. Statistical analyses of population experiment.
    • table S2. Main effect contrasts from Bayesian GLMMs.
    • table S3. Statistical analyses of the transgenerational experiment in 2014.
    • References (48–54)

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