Boron isotope sensitivity to seawater pH change in a species of Neogoniolithon coralline red alga

Abstract

The increase in atmospheric carbon dioxide (CO2) observed since the industrial revolution has reduced surface ocean pH by ~0.1 pH units, with further change in the oceanic system predicted in the coming decades. Calcareous organisms can be negatively affected by extreme changes in seawater pH (pHsw) such as this due to the associated changes in the oceanic carbonate system. The boron isotopic composition (δ 11 B) of biogenic carbonates has been previously used to monitor pH at the calcification site (pHcf) in scleractinian corals, providing mechanistic insights into coral biomineralisation and the impact of variable pHsw on this process. Motivated by these investigations, this study examines the δ 11 B of the high-Mg calcite skeleton of the coralline red alga Neogoniolithon sp. to constrain pHcf, and investigates how this taxon's pHcf is impacted by ocean acidification. δ 11 B was measured in multiple algal replicates (n = 4 to 5) cultured at four different pCO2 scenarios-averaging (± 1σ) 409 (± 6), 606 (± 7), 903 (± 12) and 2856 (± 54) μatm, corresponding to average pHsw (± 1σ) of 8.19 (± 0.03), 8.05 (± 0.06), 7.91 (± 0.03) and 7.49 (± 0.02) respectively. Results show that skeletal δ 11 B is elevated relative to the δ 11 B of seawater borate at all pHsw treatments by up to 18 ‰. Although substantial variability in δ 11 B exists between replicate samples cultured at a given pHsw (smallest range = 2.32 ‰ at pHsw 8.19, largest range = 6.08 ‰ at pHsw 7.91), strong correlations are identified between δ 11 B and pHsw (R 2 = 0.72, p < 0.0001, n = 16) and between δ 11 B and B/Ca (R 2 = 0.72, p < 0.0001, n = 16). Assuming that skeletal δ 11 B reflects pHcf as previously observed for scleractinian corals, the average pHcf across all experiments was 1.20 pH units (0.79 to 1.56) higher than pHsw, with the magnitude of this offset varying parabolically with decreasing pHsw, with a maximum difference between pHsw and pHcf at a pHsw of 7.91. Observed relationships between pHsw and calcification rate, and between pHsw and pHcf, suggest that coralline algae exhibit some resilience to moderate ocean acidification via increase of pHcf relative to pHsw in a similar manner to scleractinian corals. However, these results also indicate that pHcf cannot be sufficiently increased by algae exposed to a larger reduction in pHsw, adversely impacting calcification rates of coralline red algae. 1.0 Introduction Atmospheric CO2 has been increasing since the Industrial Revolution, from 280 ppm to more than 400 ppm today (Tans and Keeling, 2016). This increase has led to changes in ocean carbon chemistry, ultimately lowering seawater pH (pHsw) by 0.1 pH units. Climate models predict that by 2100, a high-end "business as usual" emission scenario (i.e. Intergovernmental Panel on Climate Change: Representative Concentration Pathway 8.5) will result in a global average surface pHsw of ca. 7.8, potentially reaching even lower levels at high latitudes. This large and rapid reduction in global pHsw will result in an environment that is potentially cha...

&lt;i&gt;δ&lt;/i&gt;&lt;sup&gt;11&lt;/sup&gt;B as monitor of calcification site pH in divergent marine calcifying organisms

“…For example, Cusack et al (2015) reported 30 % trigonal boron in the calcite lattice of a different species of coralline alga. Therefore, boric acid incorporation alone cannot explain the anomalously elevated δ 11 B CaCO 3 observed here for coralline algae (see also discussion in Donald et al, 2017). Moreover, although nuclear magnetic resonance spectroscopy reveals that trigonal boron is present in the calcite lattice, it cannot determine whether boric acid was incorporated directly into the calcite lattice, or if the trigonal boron originated from borate post-mineralization (e.g., see alternative mechanisms of boron incorporation discussed in Klochko, 2006;Noireaux et al, 2015).…”

“…Many calcifying marine organisms, including scleractinian corals (Al-Horani et al, 2003;Cohen and Holcomb, 2009;Cohen and McConnaughey, 2003;Rollion-Bard et al, 2003Holcomb et al, 2010;Krief et al, 2010;Trotter et al, 2011;Ries, 2011a;Anagnostou et al, 2012;Wall et al, 2016), coralline red algae (Borowitzka and Larkum, 1987;McConnaughey and Whelan, 1997;Donald et al, 2017), calcareous green algae (Borowitzka and Larkum, 1987;De Beer and Larkum, 2001;McConnaughey and Falk, 1991), foraminifera (Rink et al, 1998;Zeebe and Sanyal, 2002), and crabs (Cameron, 1985) …”

Similar controls on calcification under ocean acidification across unrelated coral reef taxa

“…It marginally decreased with seawater Ω for P. damicornis . While there are no published data of B/Ca or Raman spectroscopy for abiogenic high‐Mg calcites, both have been interpreted as carbonate system proxies in CCA (Donald, Ries, Stewart, Fowell, & Foster, ; Kamenos et al., ). We interpret B/Ca and Raman spectra as indicative of calcifying fluid DIC and calcite saturation state (Ω Cal cf ) respectively (Figure ) based on their systematics in aragonite.…”

“…Seawater Ω did not influenced DIC cf in A. yongei. In the three treatments with similar Ω, DIC cf was the highest (and B/Ca the lowest for CCA) in the treatment with elevated DIC.Mg calcites, both have been interpreted as carbonate system proxies in CCA(Donald, Ries, Stewart, Fowell, & Foster, 2017;Kamenos et al, 2013). We interpret B/Ca and Raman spectra as indicative of calcifying fluid DIC and calcite saturation state (Ω Cal cf ) respectively (…”

Ocean acidification induces subtle shifts in gene expression and DNA methylation in mantle tissue of the Eastern oyster (Crassostrea virginica)

“…Observed non-negative effects may be the result of individual resilience or the capacity of certain species to acclimatize to OA. One way this may occur is via the maintenance of pH homeostasis at the site of calcification despite an increasingly acidic environment, which is a polyphyletic response to ocean acidification (Liu et al, 2018) that has been observed in scleractinian corals (Al-Horani et al, 2002;Ries, 2011;Venn et al, 2011;McCulloch et al, 2012;Holcomb et al, 2014) , foraminifera (Rink et al, 1998;Köhler-Rink and Kühl, 2000;de Nooijer et al, 2008de Nooijer et al, , 2009 , calcareous green algae (De Beer and Larkum, 2001) , coralline red algae (Donald et al, 2017;Anagnostou et al, 2019;Liu et al, 2020) , coccolithophores (Liu et al 2018), and bivalves (Ramesh et al, 2017;Cameron et al, 2019) . In bivalves, calcification occurs within the extrapallial fluid (EPF) located between the shell and mantle epithelium, the composition of which is regulated via the active exchange of ions and other constituents through the mantle epithelium (Crenshaw and Neff, 1969;Crenshaw, 1972) .…”