Primary Life Stage Boron Isotope and Trace Elements Incorporation in Aposymbiotic Acropora millepora Coral under Ocean Acidification and Warming

Introduction

Scleractinian corals, the building blocks of coral reefs in the tropical oceans, are known for the formation of extremely productive and diverse ecosystems. These marine calcifying organisms are however threatened and in most areas in decline. The results of increasing anthropogenic CO₂ emissions are elevated sea surface temperatures (SST) and decreases in ocean pH (e.g., Pandolfi et al., 2011). Ocean acidification (OA) is the process by which the oceans take up atmospheric anthropogenic CO₂ leading to an increase in seawater H⁺ concentrations and consequently decrease in pH (Caldeira and Wickett, 2003). The effects of ocean warming or thermal stress have been widely documented in coral reefs around the world by mass coral bleachings and mortalities that are becoming more frequent and severe (Hoegh-Guldberg et al., 2007; Eakin et al., 2009; Pandolfi et al., 2011). Not only is warming impacting corals worldwide, but the effect of OA can also affect coral calcification (Gattuso et al., 1999; Kleypas et al., 1999; Anthony et al., 2008).

Declines in coral calcification over multi-decadal timescales have already been observed (De'ath et al., 2009) with further decreases projected under future climate change scenarios (Orr et al., 2005; Pandolfi et al., 2011). Reduced skeletal growth under OA conditions has been documented in corals in both natural and artificial environments (Kuffner et al., 2008; Cohen et al., 2009; Kroeker et al., 2010; Fabricius et al., 2011). Complicating the full understanding of future OA effects on ecosystems is the fact that responses vary among species; with some coral species being more resilient and less affected than others (Fabricius et al., 2011; Edmunds et al., 2012). Studies have also shown enhanced anomalous coral calcification in natural OA settings due to the combined effects of ocean warming (OW) and OA (Rodolfo-Metalpa et al., 2011).

In addition to the threat on adult corals, OA and OW can affect early-life stages of reef building species hindering coral reef sustainability. Physiological studies have shown that OA impaired coral larval metamorphosis, negatively impacted recruitment, and induced deformities in juvenile coral skeletons (Albright et al., 2010; Nakamura et al., 2011; Doropoulos et al., 2012; Foster et al., 2015, 2016). Other studies have however documented conflicting biologically-related responses such as disrupted gene expression and tolerance to the combined effects of OA and OW in juveniles or recently metamorphosed coral larvae (Moya et al., 2012; Rivest and Hofmann, 2014; Baria et al., 2015). Important questions remain for post-metamorphosis juvenile corals because studies have shown remarkable adaptability without significant effects linked to OA and OW (Chua et al., 2013a,b). Furthermore, changes in juvenile skeletal formation and geochemistry continue to be relatively unknown and unresolved.

In this study, we examined the primary polyp of the branching coral Acropora millepora to understand the effects of OA and OW on skeletal formation and geochemistry under end-of-century emission scenarios (Field et al., 2014). Our coral culture experiment provides a novel opportunity to acquire information on coral response to climate change because A. millepora have been shown to be the emerging coral model to study coral habitat degradation (Humphrey et al., 2008), elevated temperature stress (Meyer et al., 2011), genetic response to survival of combined thermal and acidification stress (Rocker et al., 2015), and possible adaptation to OA (Moya et al., 2015).

One possible tool to observe OA and the associated seawater pH change is based on the δ¹¹B composition of marine calcifiers (Hershey et al., 1986; Hemming and Hanson, 1992). The relative abundance of the two boron species in seawater, boric acid, B(OH)₃, and borate, ${\text{B}(\text{OH})}_4^{-}$, is pH dependent. Moreover, the isotopic composition and the isotopic equilibrium fractionation between the two aqueous boron species (boric acid and borate) are also pH dependent (Hershey et al., 1986; Hemming and Hanson, 1992). Based on the assumption that marine carbonates reflect the isotopic composition of ${\text{B}(\text{OH})}_4^{-}$ (Spivack et al., 1993; Palmer and Pearson, 2003), the δ¹¹B signature of marine biocarbonates such as coral aragonite skeleton have been shown to reflect seawater pH (Hönisch et al., 2004; Pelejero et al., 2005; Wei et al., 2009; Douville et al., 2010; D'Olivo et al., 2015).

The aragonite skeleton of reef-building corals such as Porites spp. and Acropora spp. have been shown to be reliable recorders of climate (e.g., SST, δ¹⁸O of seawater, etc.) (Dunbar and Wellington, 1981; Corrège, 2006; Tierney et al., 2015; Sadler et al., 2016). Coral skeletal Sr/Ca ratios are widely used for SST reconstructions with success (see reviews and compilations in Corrège, 2006; Tierney et al., 2015). The strong influence of SST on coral B/Ca and the U/Ca ratios at certain locations has also been documented (Sinclair et al., 1998; Fallon et al., 1999, 2003; Cardinal et al., 2001; Felis et al., 2010). The branching coral genus Acropora can be considered an ideal candidate for climate reconstructions because of its wide spatial distribution across the tropical oceans with long temporal range from the early-Holocene to today (Ribaud-Laurenti et al., 2001; Sadler et al., 2014). Using in situ laser ablation geochemical analyses, we measured the δ¹¹B and trace element (B/Ca, Sr/Ca, U/Ca) signatures of juvenile A. millepora (primary polyps). We aim to shed more light on the systematics and incorporation of the commonly used coral-based climate proxies in juvenile primary skeleton under the effects of OA and OW.

Materials and Methods

Experimental Setup

Fifteen adult colonies of A. millepora were collected off the coast of Orpheus Island, Australia (under GBRMPA permit No G10/33174.1) and transported within 3 h to the Marine and Aquaculture Research Facilities Unit (MARFU) at James Cook University in Townsville, Australia. The colonies were maintained in outdoor flow-through aquaria filled with 5 μm filtered seawater resulting in the absence of zooxanthellae endosymbionts for coral colonization (Figure 1). The exclusion of these microorganisms limits our impact observations to the coral host animal itself without the complications of zooxanthellate endosymbionts involvement (e.g., photosynthesis, lipids production, etc.).

FIGURE 1

Figure 1. Schematic representation of the experimental design. Adult coral colonies were collected and placed in filtered seawater (5 μm) followed by spawning and fertilization. The embryos (Day 0) were immediately transferred to seawater that had been equilibrated with air containing 390 μatm and 750 μatm pCO₂, reflecting the control and acidification condition under medium CO₂ scenario for the twenty-first century (Field et al., 2014). Under each pCO₂ condition, two seawater temperatures were made: 27°C and 29°C. Metamorphosis of the Acropora millepora was induced (Day 5) after fertilization by the introduction of unglazed terracotta tiles conditioned with crustose coralline algae under ambient seawater conditions. At the end of the experiment after exposure (Day 10), the primary A. millepora polyps were collected and air-dried for preservation. Larval developmental stage sketches modified from Moya et al. (2015).

Immediately after spawning, eggs and sperm were collected and transferred into fertilization tanks. Once fertilized (i.e., 2-cell stage), the embryos were transferred and kept for 10 consecutive days in experimental tanks that were previously equilibrated at four different conditions. The four experimental conditions were as follows: (1) 390 μatm pCO_2(air) at 27°C (control condition), (2) 390 μatm pCO_2(air) at 29°C, (3) 750 μatm pCO_2(air) at 27°C, and (4) 750 μatm pCO_2(air) at 29°C. CO₂ concentration was produced and regulated using a CO₂ mixing system developed by Munday et al. (2009). A schematic summary of the experimental setup can be found in Figure 1.

All seawater measurements such as pH (NBS scale, Hach HQ11D, calibrated daily), temperature (°C), and Total Alkalinity (A_T) were monitored daily at 11:00 over the duration of the experiment. Mean seawater chemistry parameters [pCO_2(seawater), carbonate ion (${\text{CO}}_3^{2-}$), and aragonite saturation state (Ω_Aragonite)] were estimated using CO2SYS version 2.1 (Lewis and Wallace, 1998) with salinity of 35 using dissociation constants from Mehrbach et al. (1973) and refitted by Dickson and Millero (1987) with boron source of Uppstrom (1974) (Table 1).

TABLE 1

Table 1. Acropora millepora juvenile coral experimental conditions and parameters.

Metamorphosis of the A. millepora larvae into coral juveniles of a single corallite or primary polyp juveniles occurred within the water column of the aquaria after 5 days leading to fully developed calcification over the duration of the experiment (Figure 1). Metamorphosis was induced by the introduction of unglazed autoclaved terracotta tiles that had been conditioned with crustose coralline algae under ambient seawater conditions (Heyward and Negri, 1999). After 10 days of exposure to experimental conditions (5 days post-metamorphosis), the coral juveniles from the four experimental conditions were collected (Figure 1). The samples were left to dry in sample tubes at room temperature and transported to Laboratoire d'Océanographie et Climat (LOCEAN) at the Institut de Recherche pour le Développement (IRD) Centre France-Nord in Bondy, France.

A. millepora primary polyp juveniles were randomly picked from each individual experimental condition and pretreated with 50% NaOCl for up to 72 h to remove the organic matter (coral tissues). The primary polyp juveniles were then placed in 18.2 MΩ Milli-Q water for cleaning overnight. Pretreatment of samples by NaOCl is a common procedure that has no influence on microstructure and trace element or boron isotope geochemistry (Watanabe et al., 2001; Nothdurft and Webb, 2007; Holcomb et al., 2015).

Laser Ablation—ICP-MS and—MC-ICP-MS Analyses

Trace element analyses on the cleaned primary polyp juveniles were completed by laser ablation (ESI NWR-213nm; Nd:YAG Laser) coupled to an Agilent 7500cx Quadrupole Inductively Coupled Plasma Mass Spectrometer (LA-ICP-MS) on the ALYSES Analytical Platform (IRD/UPMC) at LOCEAN. Trace element measurements by LA-ICP-MS has been shown to be both precise and accurate at the micron-scale (Sinclair et al., 1998; Fallon et al., 1999). This technique was chosen for this study because of the limited size and number of primary polyp juvenile corals. The operational repetition rate frequency of the laser was 10 Hz and 5 mJ for laser power with sample introduction to the ICP-MS by helium mixed with argon prior to reaching the plasma torch (Table 2). Each LA-ICP-MS analysis was completed as a single laser spot of 40 μm (beam diameter) on the surface of the primary polyp juvenile with a laser dwell time (acquisition time) of 50 s. Washout time between each laser spot analysis was 60 s (Table 2). Eight seconds of gas blank was measured before the initiation of each laser analysis. Daily adjustments of the LA-ICP-MS were done using the NIST SRM 610 standard (glass matrix standard reference material).

TABLE 2

Table 2. Laser ablation ICP-MS and MC-ICP-MS instrumental setup.

The δ¹¹B ratio analysis on the same samples were performed by laser ablation (ESI NWR-193 nm; ATLEX 300SI Laser) coupled to a Thermo Scientific Neptune Plus Multi-Collector ICP-MS (LA-MC-ICP-MS) at the Laboratoire des Sciences du Climat et de l'Environnement (LSCE), Gif-sur-Yvette, France. The thorough laser application δ¹¹B ratio analysis methodology including accuracy and precision using this instrumentation has been previously documented on a Porites sp. coral (Thil et al., 2016). The laser spot mode was used with a repetition rate frequency of 15 Hz, 7 mJ for laser energy, beam diameter of 100 μm, and a laser dwell time of 60 s (Table 2). Washout time between each laser spot analysis was 40 s (Table 2). Daily adjustments of the LA-MC-ICP-MS were optimized using the NIST SRM 612 standard (glass matrix standard reference material).

Each primary polyp juvenile was analyzed at three carefully chosen locations on the skeleton for trace elements determination and three additional locations for δ¹¹B signature (6 total laser spot analyses per juvenile). The laser was triggered on a location where at least 90% of the laser field contained skeletal material to have a more robust analytical signal because the primary polyp (single corallite) juveniles are porous (Figure 2). The total number of juveniles analyzed varied between conditions, with a minimum of 10 individuals per condition, producing a minimum of 30 trace element and 30 δ¹¹B ratio measurements per condition.

FIGURE 2

Figure 2. Photographs of representative individual primary polyp A. millepora juvenile corals (single corallite) cultured in the four experimental conditions (Table 1). (A,B) Condition 1 (control) revealing normal skeletal material. (C,D) Condition 2 with more translucent skeletal characteristics relative to condition 1. (E,F) Condition 3 with decreased bulk volume and skeletal material. (G,H) Condition 4 with more asymmetrical, translucent, and brittle skeletal material. All scale bars are 500 μm.

The main criteria for our laser ablation results were: (a) each juvenile must have three complete laser spots, (b) each laser spot's analytical signal is constant over time, and (c) each measurement is above the limits of detection for the investigated element. Results for an individual juvenile were rejected if there was an incomplete measurement from any of the three laser spots. With these criteria for trace elements, 15 juveniles were analyzed for condition 1 (number of laser spots, n = 45), 22 for condition 2 (n = 66), 20 for condition 3 (n = 60), and 22 for condition 4 (n = 66). For the δ¹¹B ratio, 10 juveniles were analyzed for condition 1 (number of laser spots, n = 30), 10 for condition 2 (n = 30), 14 for condition 3 (n = 42), and 13 for condition 4 (n = 39).

Repeated measurements of the international standards NIST SRM 610 (trace elements) or NIST SRM 612 (boron isotopes) were completed under the same conditions (e.g., laser spot size, frequency, etc.) for instrumental drift correction and precision assessment and verification. The inter-laboratory calibration coral standard JCp-1 (Porites coral) (Okai et al., 2002; Hathorne et al., 2013) was also measured for comparison. Measurements of the JCp-1 sample was derived from pressed individual pellets made of 500 mg of JCp-1 powder under a 10 ton cm⁻² force following the description of Lazareth et al. (2007). Additionally, a Porites sp. coral section of known δ¹¹B ratio (Thil et al., 2016) was also repeatedly measured on the MC-ICP-MS for baseline verification.

Daily LA-ICP-MS data processing and correction for machine drift was completed using the GLITTER software (Van Achterbergh et al., 2001). We chose the most stable signal integration time (15–40 s) with ⁴³Ca as the internal standard with 40 wt % Ca content and gas blank removed from each signal. The NIST SRM 610 glass standard was used as the external standard to calculate quantitative element concentration of the unknown coral juveniles using concentrations of Pearce et al. (1997).

LA-ICP-MS results are presented in element/Ca ratios for conventional coral geochemistry-based paleoclimatology comparison. LA-ICP-MS precision of NIST SRM 610 is within the certified/suggested values and reported errors in Pearce et al. (1997) (mean ± 1σ standard deviation, SD; % relative standard deviation, RSD): 17.402 ± 0.394 mmol mol⁻¹ for B/Ca (2.27% RSD), 3.041 ± 0.032 mmol mol⁻¹ for Sr/Ca (1.06% RSD), and 1031.823 ± 14.809 μmol mol⁻¹ for U/Ca (1.43% RSD). Repeated analysis of the international coral standard JCp-1 (carbonate powder) pressed pellet for trace elements are 0.577 ±0.056 mmol mol⁻¹ for B/Ca (9.67% RSD), 9.484 ± 0.266 mmol mol⁻¹ for Sr/Ca (2.81% RSD), and 1.233 ± 0.109 μmol mol⁻¹ for U/Ca (8.27% RSD). The published robust average and SD of the JCp-1 standard measured in solution are 0.459 ± 0.022 mmol mol⁻¹ for B/Ca, 8.838 ± 0.042 mmol mol⁻¹ for Sr/Ca, and 1.192 ± 0.045 μmol mol⁻¹ for U/Ca (Hathorne et al., 2013). The inter-laboratory offset and larger SD of the JCp-1 standard is due to differences in analytical techniques between solution- and laser ablation-based measurements. No corrections were applied to our results with the published values of JCp-1 because of (a) the large heterogeneity of the powder pellet analyzed under laser ablation compared to solution-based results and (b) our goal to focus on the relative changes and differences between experimental conditions and not in the reconstruction of absolute SST.

The δ¹¹B ratio LA-MC-ICP-MS analysis results are reported in ‰ deviation compared to the published JCp-1 value (24.3‰) as reference (Foster et al., 2013) allowing us to obtain a low 2σ SD (±0.38‰; n = 47) within the published 2σ SD. The 2σ SD of repeated analyses of the international certified NIST SRM 612 silicate glass matrix (Brand et al., 2014) was ±0.88‰ (n = 23). The analyzed internal laboratory standard (Porites coral slab section) δ¹¹B ratio was homogeneous (20.69‰) with a low 2σ SD (±0.47‰; n = 47). Daily data processing and correction were based on a combination of our in-house Porites sp. sample (Thil et al., 2016) and the JCp-1 standard.

Estimation of Seawater pH and Statistical Analyses

The estimation of seawater pH values (Total scale) was calculated from the primary polyp juvenile δ¹¹B ratios following established equation (e.g., Zeebe et al., 2001).

$\begin{array}{l}p{H}_{sw}=p{K}_B-\text{log}[\left({\delta }^{11}{B}_{sw}-{\delta }^{11}{B}_c\right)/\\ \left\{{\alpha }_{\left[B3-B4\right]}{\delta }^{11}{B}_c-{\delta }^{11}{B}_{sw}+{10}^3\left({\alpha }_{\left[B3-B4\right]}-1\right)\right\}]\end{array}$

The parameters of Equation (1) are as follows: pK_B (8.57 at 27°C, 8.55 at 29°C, and salinity of 35) (Dickson, 1990) is the equilibrium constant for boron in seawater; α_[B3−B4] is the fractionation factor for isotope exchange between B(OH)₃ and ${\text{B}(\text{OH})}_4^{-}$ in seawater; the δ¹¹B_sw (39.61‰) (Foster et al., 2010) and δ¹¹B_c represent the δ¹¹B in seawater and coral, respectively. For this study, we chose the fractionation factor α_[B3−B4] of 1.0272 from the empirical study of Klochko et al. (2006), which has been confirmed to be between the coral species-specific values range of 1.026–1.028 (Trotter et al., 2011; McCulloch et al., 2012) and applied in many studies (Allison et al., 2010; Krief et al., 2010; Rollion-Bard et al., 2011; Dissard et al., 2012).

Statistical analyses for this study were completed using the Stats package in R (R Development Core Team, 2013). An assessment of the normality of our data was verified graphically and we used a two-way crossed analysis of variance test (ANOVA) to highlight potential effects of OA, OW, and the interactions between the two factors on coral geochemical composition. When differences were significant, a post-hoc Student's T-test was applied. Mean and standard deviation (or error) are presented.

Results and Discussion

A. millepora Primary Polyp Juvenile Morphology

Visual inspections of our coral juvenile skeletons revealed pronounced morphological differences among the experimental treatments of temperature and pCO₂ (Figure 2). As our cultured primary polyp juveniles metamorphosed within the water column, they are different than those found in the field that metamorphosed on settlement substrates. Condition 1 (27°C and 390 μatm pCO₂) and condition 2 (29°C and 390 μatm pCO₂) retained the most symmetrical structure representing normal to near-normal growth (Figures 2A–D). Exposure to OW alone (condition 2; Figures 2C,D) did not produce skeletal materials that are noticeably different to the control condition (Figures 2A,B).

For conditions 3 (27°C and 750 μatm pCO₂) and 4 (29°C and 750 μatm pCO₂), we observed pronounced morphological changes relative to the control. Juveniles of conditions 3 and 4 under OA showed notable stunted asymmetrical growth. The juveniles were notably smaller in overall size with translucent skeletal materials that were brittle and prone to breakage (Figures 2E–H). The lack of visual difference between conditions 1 and 2 is likely reflecting the large temperature tolerance range of this species in nature. In contrast, the asymmetrical growth and microstructure abnormalities of conditions 3 and 4 are common OA stress features in juvenile corals (Cohen et al., 2009; Foster et al., 2015, 2016). With sample picking procedure being equal across all conditions, the brittle and disintegrating nature of the juvenile skeletons under OA and OW is not an artifact of sample handling. Instead, this reflects the inability of the juvenile A. millepora coral to build normal skeletons. The findings of the fragile nature of the skeleton and abnormal growth of our coral juveniles are in agreement with previously observed effects on other cultured tropical coral juveniles (Cohen et al., 2009; Foster et al., 2015, 2016).

Scanning Electron Microscopy (SEM) observations confirmed our morphological observations (Figure 2) of OA and OW impact on the primary polyps early-life growth stage with more compact or stunted growth leading to smaller overall polyp size (Figure 3). A. millepora primary polyp calcification at this early-life growth stage in all conditions produced shingle-like aragonite. The proto-aragonite appears prior to the development of the acicular crystals organization, which is interspersed with more developed aragonite crystals. The crystal habit resulted in an aggregate formation resembling fish scale-like morphology, which has been previously described in Acropora spp. coral recruits (Gladfelter, 1983, 2007; Van de Locht et al., 2013). Centers of calcification (COC or Early Mineralization Zones) and fasciculi (fibrous aragonite) bundles can be observed in all conditions. The COC is the biomineralization structure or setting of coral skeleton that is surrounded by the fibrous aragonite bundles (fasciculi; Figure 4). The stunted growth of conditions 3 and 4 resulting from OA impact appears to have reduced or impeded the spread (extension) of the fasciculi between the COCs, creating tighter or more compact assemblages of COC (Figures 3, 4). The abnormal stunted growth at low pH has been shown to be a result of microstructure differences with more COC relative to fasciculi content under high pCO₂ (Hennige et al., 2015). Furthermore, disorganized carbonate precipitation such as disordered aggregate of highly faceted rhombs have been reported (Cohen et al., 2009). Larger spacing between aragonite crystals of the fasciculi can be observed in the primary polyps under OA resulting in more divided aragonite crystals than at ambient pCO₂ (Figure 4). Such microstructure changes in the early-life stage of tropical corals have undeniable consequences on the geochemical proxy records as discussed below, in agreement with previous studies (Cohen et al., 2009).

FIGURE 3

Figure 3. Representative Scanning Electron Microscopy results of primary polyp A. millepora juvenile corals. Each row of images is grouped by experimental condition, which are stated above the row and shown from left to right. Each image is a distinct A. millepora primary polyp that has been analyzed by laser ablation for this study. Most A. millepora individuals are shown with oral cavity in the center of the image or placement on its side. The normal, near symmetrical morphology of the primary polyps of conditions 1 and 2 are shown in the top two rows. The asymmetrical morphology of primary polyps of conditions 3 and 4 with impacted stunted and retarded growth are shown in the bottom two rows. All scale bars are 100 μm.

FIGURE 4

Figure 4. High magnification Scanning Electron Microscopy results of primary polyp A. millepora juvenile corals. Each row of images is grouped by experimental condition, which are stated above the row and shown from left to right. Every image is a distinct A. millepora primary polyp that has been analyzed by laser ablation for this study. Skeletal microstructure features such as clear centers of calcification (coc) and fasciculi bundles (fas) composed of primary aragonite crystals (arag) can be seen throughout all four experimental conditions. The primary aragonite crystals (arag) of the primary polyps are predominantly orientated in a scale-like aragonite formation (sc) with newer growth layering on top of older growth. Less developed proto-aragonite (par) shingles prior to fine crystals development and presence of disorganized aragonite (da) are more prevalent in the OA conditions.

We are aware that since our corals were aposymbiotic or raised without endosymbionts, our morphological observations may have over-simplified the combined effects of elevated CO₂ and temperature change. Various studies with A. millepora coral with endosymbionts have shown acclimation possibilities that can range from gene regulation of calcification to metabolism (Strahl et al., 2013; Rocker et al., 2015). Thus, the ability and role of symbiotic zooxanthellae to mitigate A. millepora coral stress cannot be discounted. Endo- and ecto-symbionts such as cyanobacteria (Lesser et al., 2004) and microboring algae (Fine and Loya, 2002; Verbruggen and Tribollet, 2011) have also shown notable OA and OW mitigating roles.

δ¹¹B Signature of A. millepora Primary Polyp and Reconstructed pH

Mean intra-coral reproducibility for the δ¹¹B ratio ranged between ±0.52 to ±0.86‰ (Table 3) and was within the δ¹¹B ratio 2σ SD analytical error. The juvenile A. millepora coral δ¹¹B ratio indicates a consistent relationship to the increase in water temperature (Figure 5A). Coral juveniles cultured under the same pCO₂ (390 μatm) but different water temperatures had significantly lower mean δ¹¹B ratios at low temperature (27°C, 21.79 ± 1.61‰) than high temperature (29°C, 23.41 ± 0.92‰; T-test, p = 1.70 × 10⁻³; Figure 5A; Tables 4, 5). The same was observed between conditions 3 and 4 cultured under high pCO₂ condition (750 μatm) with significantly lower δ¹¹B ratios at 27°C (19.18 ± 2.63‰) than at 29°C (22.53 ± 1.57‰; T-test, p = 2.81 × 10⁻³; Figure 5; Tables 4, 5). The analysis of variance (ANOVA) showed that the δ¹¹B ratio was significantly influenced by the expected impact of pCO₂ [F_{(1, 68)} = 10.402, p = 2.41 × 10⁻³] and water temperature [F_{(1, 68)} = 23.895, p = 1.46 × 10⁻⁵; Table 6].

TABLE 3

Table 3. Primary polyp juvenile A. millepora reproducibility in each experimental condition.

FIGURE 5

Figure 5. Box-whisker plots of the primary polyp A. millepora juvenile corals geochemical results. In each plot from left to right are the respective experimental conditions (e.g., Condition 1, C1). (A) δ¹¹B (‰), (B) B/Ca (mmol mol⁻¹), (C) Sr/Ca (mmol mol⁻¹), and (D) U/Ca (μmol mol⁻¹). The box plots represent the lower and upper quartiles with the median shown as a horizontal line within each box. The top and bottom whiskers extending from the box plots represent the highest and lowest values respectively. The mean and analytical errors for the NIST SRM 610 and JCp-1 standards measured by LA-ICP-MS are – B/Ca: 17.402 ± 0.394 mmol mol⁻¹ (2.27% RSD; NIST 610) and 0.577 ±0.056 mmol mol⁻¹ (9.67% RSD; JCp-1); Sr/Ca: 3.041 ± 0.032 mmol mol⁻¹ (1.06% RSD; NIST 610) and 9.484 ± 0.266 mmol mol⁻¹ (2.81% RSD; JCp-1); U/Ca: 1031.823 ± 14.809 μmol mol⁻¹ (1.43% RSD; NIST 610) and 1.233 ± 0.109 μmol mol⁻¹ (8.27% RSD; JCp-1). The numbers above each experimental condition indicate the significant difference in means from Student's T-test (p < 0.01; Table 5).

TABLE 4

Table 4. Summary of mean primary polyp juvenile coral analyses in each experimental condition.

TABLE 5

Table 5. Summary of Student's T-test results (p-values) between each experimental condition.

TABLE 6

Table 6. Summary of primary polyp juvenile coral two-way (crossed factors) analysis of variance (ANOVA).

The estimation of pH (see Section Estimation of Seawater pH and Statistical Analyses; e.g., Zeebe et al., 2001) using the pK_B of 8.57 at 27°C and 8.55 at 29°C (Dickson, 1990), the fractionation factor (α_[B3−B4]) of 1.0272 (Klochko et al., 2006), and our primary polyp juvenile coral δ¹¹B ratios revealed a pH difference of 0.09 pH units (Total scale) between the control (pH = 8.32) and condition 2 (pH = 8.41). The pH difference is even larger at 0.23 pH units between condition 3 (8.12) and 4 (8.35). The offset between the control condition's reconstructed pH of 8.32 and the measured culture system seawater pH of 7.94 (Total scale converted from the measured pH of 8.08 in NBS scale; Table 1) may be due to the choice of boron isotope fractionation factor (α_[B3−B4]) (Hönisch et al., 2004). But is more likely indicating the difference between seawater and skeletal δ¹¹B and pH variations at the site of calcification or calcification space (Trotter et al., 2011; McCulloch et al., 2012).

The range of offset, 0.38–0.56 pH units, between skeletal reconstructed pH from our primary polyp juveniles and the surrounding seawater pH is supported by the similarly elevated extracellular pH range (0.2–0.5) measured in coral calcifying space relative to seawater pH in other corals (Venn et al., 2011; McCulloch et al., 2012). Microelectrode pH measurement profiles inside adult polyps of A. millepora coral colonies also indicate a 0.5 pH units increase in interior calcification space pH (8.65) relative to seawater pH (8.15) (Cai et al., 2016). These differences between outside seawater pH and internal calcification space pH are comparable to our reconstructed δ¹¹B-pH and measured seawater pH difference average of 0.43 pH units. Furthermore, high-resolution pH imaging of primary polyp juveniles of aposymbiotic A. digitifera indicated active pH up-regulation at the site of calcification (Ohno et al., 2017). Our results confirm these observations in that our coral species also has a well-regulated internal pH at the calcification sites, which is considerably higher than the external seawater pH.

The impact of higher temperature on our A. millepora primary polyp resulted in the enrichment of δ¹¹B causing an increase in reconstructed pH by at least 0.09 pH units (conditions 1 and 2) and 0.23 pH units (conditions 3 and 4). The relationship between temperature and pH at equilibrium is well known, i.e., when the temperature in solution increases, the ability of the water to ionize increases so does the concentration of H⁺ ions in solution, leading to a decrease in pH. Without this inherent relationship between temperature and pH, and thus δ¹¹B, the results of conditions 1 and 2 as well as conditions 3 and 4 would have been expected to be more similar with no significant difference between the means. Our observations confirm a previous study with cultured Acropora sp. coral nubbins (adult branches) with similar enrichment of skeletal δ¹¹B ratio due to increasing temperature reflecting behavior changes at the calcification site possibly due to metabolic processes (Dissard et al., 2012). Our microstructure analysis indicates that biomineralization was compromised due to prolonged stress exposure in conditions 3 and 4 (Figure 4). The primary polyps of conditions 3 and 4 both contained less bundled (more between crystal spacing) aragonite habits resembling more disorganized orientation of crystals than the conditions at ambient pCO₂. These skeletal features of the primary polyp juveniles may be indicating, in the absence of endosymbionts, the coral only acclimation processes to stress or the attempt to counteract the impact of increased acidification. This response also likely increased the pH up-regulation resulting in a reconstructed pH (8.35, condition 4) that is even more elevated than the control condition (8.32). The enrichment of the δ¹¹B ratio (conditions 2 and 4), is likely related to metabolic processes of the A. millepora juveniles and further support the conclusion that certain coral species have the ability to adapt to increasing OW and OA by up-regulating its internal pH (McCulloch et al., 2012; Ohno et al., 2017). We thus provide additional evidence of pH homeostasis or elevated pH control in scleractinian corals even at the primary polyp juvenile life-stage subjected to OA and OW.

Moreover, a recent study of coral calcifying space pH revealed significant influence and modulation of internal pH due to photosynthesis and respiration (Comeau et al., 2017) that was alluded to by Dissard et al. (2012). The effects of elevated pCO₂ on coral photosynthesis has been reported in previous studies, which have suggested a variety of effects that ranged from inhibitory to stimulatory (Reynaud et al., 2003; Anthony et al., 2008; Kaniewska et al., 2012). Since our primary polyp juveniles were raised without endosymbionts, we are restricted to the discussion of coral animal metabolism or dark respiration. Studies with adult A. millepora (Kaniewska et al., 2012) and larvae of Porites spp. (Albright and Langdon, 2011; Rivest and Hofmann, 2014) have all indicated significantly decreased coral respiration due to elevated pCO₂. In adult A. millepora, the impact can even be observed prior to biomineralization (Kaniewska et al., 2012). Thus, the metabolic effects of elevated pCO₂ that in turn increased the cost of calcification (McCulloch et al., 2012) cannot be dismissed. This higher cost of calcification is implied from our observations of conditions 3 and 4 that precipitated less fasciculus between the COCs and with more disorganized aragonite aggregation (Figure 4). The increase in pCO₂ thus suggests a direct impact of retarded coral calcification related to coral respiration with associated pH up-regulation.

Primary Polyp A. millepora Skeletal Sr/Ca as SST proxy

Mean intra-coral reproducibility of the Sr/Ca ratios are within the 1σ SD analytical error of the JCp-1 coral standard (Table 3). The difference between Sr/Ca ratio means at low pCO₂ but different temperatures (conditions 1 and 2) was not significant. The large inter-coral Sr/Ca range within these two conditions contributed to this result (Figure 5; Table 4). Across the high pCO₂ conditions, the mean Sr/Ca ratio of condition 3 (27°C) was significantly higher than condition 4 (29°C; T-test, p = 5.62 × 10⁻⁶; Table 5). Using published Acropora sp. Sr/Ca-SST sensitivity of −0.04 and −0.05 mmol mol⁻¹ °C⁻¹ (Xiao et al., 2014; Sadler et al., 2016), the 2°C experimental difference between conditions 1 (mean = 9.975 mmol mol⁻¹) and 2 (mean = 9.798 mmol mol⁻¹) would equate to a difference of 3.54 or 4.42°C. Similarly, the difference between conditions 3 (mean = 9.674 mmol mol⁻¹) and 4 (mean = 9.432 mmol mol⁻¹) would equate to a difference of 4.84 or 6.05°C. Our interpretation and discussion are limited by the experimental design consisting of only two temperatures and lacking a full robust temperature calibration range. Nevertheless, the fidelity of the Sr/Ca-SST proxy using A. millepora juvenile skeleton at just 2°C warming is uncertain and the results indicate possible bias of reconstructed SST. Even though the Sr/Ca-SST sensitivities used for the A. millepora primary polyp juvenile coral may be unsuitable because of the known requirement for species-specific calibrations and possible differences between adults and juveniles. It does however provide a quasi-benchmark on the possibilities for erroneous SST reconstructions using these current Sr/Ca-SST sensitivity calibrations.

Examination of the same temperature (27°C) but different pCO₂ revealed significant difference between the Sr/Ca means of condition 1 and conditions 3 (T-test, p = 0.0011; Figure 5; Tables 4, 5). Likewise, the mean Sr/Ca ratio of condition 2 was significantly different when compared to condition 4 of the same temperature (29°C) but different pCO₂ (T-test, p = 8.98 × 10⁻⁸; Figure 5; Tables 4, 5). These results indicate that the primary polyp juvenile coral Sr/Ca ratio is not only significantly impacted by temperature [ANOVA, F_{(1, 68)} = 20.088, p = 5.41 × 10⁻⁵; Table 6] but also by pCO₂ [ANOVA, F_{(1, 68)} = 43.395, p = 5.11 × 10⁻⁸; Table 6]. The significant impact of OA at 29°C indicates the possibility of inaccurate coral-based SST reconstruction. The difference of 0.37 mmol mol⁻¹ between conditions 2 and 4 at 29°C would equate to a difference of +7.4 or +9.2°C in reconstructed SST due to OA.

Bias of reconstructed SST from coral Sr/Ca under OA has been previously documented (Tanaka et al., 2015; Cole et al., 2016). Our findings of a SST warm bias (low Sr/Ca) between conditions 1 and 3 as well as conditions 2 and 4 are not in agreement with the SST cold bias (high Sr/Ca) results found by Tanaka et al. (2015) and Cole et al. (2016). Studies with cultured Pacific Porites spp. and Acropora digitifera and Atlantic Favia fragum have shown increase in Sr/Ca ratio (colder reconstructed SST) due to increase in pCO₂, declining aragonite saturation, or decrease pH (Cohen et al., 2009; Tanaka et al., 2015; Cole et al., 2016). On the contrary, our results with aposymbiotic A. millepora primary polyp revealed a consistent decrease of the Sr/Ca ratio (warming bias) under OA conditions. Biases and inaccuracies in Sr/Ca-SST reconstructions have been attributed to calcification and growth-related factors with suggestions for growth-related rescaling procedures (Gagan et al., 2012). Sr/Ca ratio in corals has also been shown to vary across different skeletal materials and is inherently heterogeneous due to differences in growth (Bagnato et al., 2004; Giry et al., 2010; DeLong et al., 2011).

The microstructure examinations revealing more COC content relative to fasciculi under high pCO₂ cannot explain the decrease in Sr/Ca or reconstructed SST bias because studies have demonstrated that coral COC content results in higher Sr/Ca than fasciculi (Allison et al., 2005; Meibom et al., 2006, 2008). This is in contrast to our geochemical and microstructure findings. Furthermore, we did not observe any secondary aragonite precipitation and dissolution that can alter the Sr/Ca ratio where both of these factors are consistently associated with higher Sr/Ca ratios (cooling bias) (Hendy et al., 2007). Species-specific impact on skeletal Sr incorporation from OA have been observed with no significant impact on Montipora capitata Sr/Ca (Kuffner et al., 2012) but significant in other Pacific species (Porites spp. and A. digitifera) (Tanaka et al., 2015; Cole et al., 2016). Therefore, the bias (lower Sr/Ca) and impact of OA observed in our A. millepora primary polyps may be representing hindered early-life stage biomineralization and aragonite precipitation processes.

Relationship of Primary Polyp A. millepora Skeletal B/Ca and U/Ca

Mean intra-coral reproducibility of the B/Ca ratio is satisfactory (Table 3) and within the 1σ SD analytical error of the JCp-1 coral standard. The primary polyp juveniles cultured at 390 μatm at both temperatures had lower mean B/Ca values than juveniles cultured at 750 μatm at both temperatures (Figure 5; Table 4). The mean B/Ca of condition 1 (Figure 5; Table 4) was not significantly different to that in condition 2 (Table 5). Mean B/Ca of condition 3 was also not significantly different to that in condition 4 (Figure 5; Tables 4, 5). The B/Ca ratios did not indicate a temperature effect as observed in the δ¹¹B signature. This is confirmed as our B/Ca ratio was only significantly affected by changes in pCO₂ concentration [ANOVA, F_{(1, 68)} = 17.808, p = 1.24 × 10⁻⁴; Table 6] and not temperature (Figure 5; Table 6). Our primary polyp juveniles result is in contrast to studies that have found both significant inverse (Fallon et al., 2003) and direct (Dissard et al., 2012) relationships between B/Ca and SST in tropical corals.

Related to the lack of B/Ca correlation to temperature, our primary polyp juvenile corals also do not provide any evidence of a direct relationship between B/Ca and Sr/Ca, contrary to other studies (Sinclair et al., 1998; Fallon et al., 1999; Figures 6A,B). Studies using tropical coral species have indeed reported positive correlations between B/Ca and Sr/Ca indicating a coupled relationship to temperature (Fallon et al., 2003; Allison et al., 2010). Comparison to calculated seawater [${\text{CO}}_3^{2-}$] (low [${\text{CO}}_3^{2-}$] at high pCO₂ and higher [${\text{CO}}_3^{2-}$] at low pCO₂; Table 1) support our finding that B/Ca ratios are not significantly different between conditions of the same pCO₂ with different temperatures (Figure 7A). It is only significantly impacted by pCO₂ and not water temperature. Instead, our primary polyp juvenile B/Ca results are reflecting the large day-to-day fluctuations of seawater pCO₂ and related [${\text{CO}}_3^{2-}$] over the 10-day period (Table 1; Figure 7A). A recent synthetic aragonite study corroborates this conclusion since it was demonstrated that aragonite B/Ca ratio can be used to estimate [${\text{CO}}_3^{2-}$] as it is principally a function of [${\text{B}(\text{OH})}_4^{-}$]/[${\text{CO}}_3^{2-}$]^0.5 (Holcomb et al., 2016).

FIGURE 6

Figure 6. Sr/Ca and U/Ca ratios relationship to B/Ca ratio in primary polyp A. millepora juvenile coral. The Sr/Ca (mmol mol⁻¹) and U/Ca (μmol mol⁻¹) plots are oriented based on pCO₂ concentration with the left column for the experiments at 390 μatm pCO₂ and the right column for the conditions at 750 μatm pCO₂. (A) Sr/Ca and B/Ca ratios of condition 1 (blue triangle) and condition 2 (red triangles), (B) Sr/Ca and B/Ca ratios of condition 3 (blue circles) and condition 4 (red circles). Note that Sr/Ca ratios are inversely plotted to reflect the temperature relationship of lower (higher) Sr/Ca with higher (lower) temperature. (C) U/Ca and B/Ca ratios of condition 1 (blue triangle) and condition 2 (red triangles), (D) U/Ca and B/Ca ratios of condition 3 (blue circles) and condition 4 (red circles). Correlation relationships between U/Ca and B/Ca are shown in respective colors with Pearson Product Moment correlation coefficients listed indicating strength of association and significance (p < 0.01). The 1σ standard deviation (SD) of the measured NIST SRM 610 and JCp-1 coral standard for trace element/Ca ratios are listed in Figure 5.

FIGURE 7

Figure 7. Measured B/Ca and U/Ca ratios relationship to calculated seawater $\left[{\text{CO}}_3^{2-}\right]$. Mean and 1σ standard deviation of (A) B/Ca (mmol mol⁻¹) and (B) U/Ca (μmol mol⁻¹) in primary polyp A. millepora juvenile coral in each of the four experimental conditions comparison to calculated seawater carbonate ion (${\text{CO}}_3^{2-}$) from CO2SYS (Table 1).

Growth and morphological differences may explain the contrast in B/Ca changes related to the variations in microstructure and in proportions of COC and fasciculi. Our B/Ca results (Figure 5) are in agreement with morphological observations that under OA conditions, the juvenile coral skeletal materials contain less of the fast growth fasciculi relative to the slower growth COCs and vice versa at ambient pCO₂ (Figure 4). Under normal conditions, coral B/Ca ratios are higher in COC than fasciculi in tropical reef corals (Meibom et al., 2006). This is confirmed by our SEM analysis that indicated low pCO₂ conditions produced more visible fasciculi than COCs while OA conditions resulted in more compacted skeletal morphology and decrease in skeletal surface area (less fasciculi and more COC) with disordered aragonite organization. Thus, our result of lower B/Ca ratios is in agreement with skeletal materials containing more fasciculi content relative to COC (Meibom et al., 2006).

Mean intra-coral reproducibility of U/Ca ratios are within the 1σ SD analytical error of the JCp-1 coral standard (Table 3). U/Ca ratios in our primary polyp juveniles do not contain a relationship to SST as previous studies have suggested (Min et al., 1995; Cardinal et al., 2001; Armid et al., 2011). In general, the U/Ca ratio was lower (higher) at low (high) pCO₂ (Figure 5; Table 4). The mean U/Ca of condition 1 was not significantly different than the means of condition 2. It is possible that the 2°C temperature change was within the range of tolerance of A. millepora, which did not permit the detection of a temperature effect in U/Ca. Surprisingly, the means of U/Ca in conditions 2 and 3 were not significantly different. In fact, the only mean significance found was between the low means of condition 2 (0.940 ± 0.058 μmol mol⁻¹; Figure 5) and high means of condition 4 (1.008 ± 0.073 μmol mol⁻¹; T-test, p = 1.63 × 10⁻³; Table 5) for cultures at the same elevated temperature (29°C) but different pCO₂.

Of the measured trace elements in the A. millepora juvenile coral skeletal material, only U/Ca and B/Ca under high pCO₂ conditions contain occurrence of correlated relationships (Figures 6C,D). This is not entirely unexpected as U/Ca in zooxanthellate and azooxanthellate corals have been shown to be influenced by pH (Inoue et al., 2011; Raddatz et al., 2014). Our results partially support this conclusion that the larger change in pCO₂ decrease (increasing OA, decreasing pH) and associated [${\text{CO}}_3^{2-}$] induces the only significant impact on U/Ca ratio [ANOVA, F_{(1, 68)} = 8.730, p = 0.005; Table 6]. U/Ca in marine biogenic carbonates has been shown to be related to [${\text{CO}}_3^{2-}$] of the carbonate system (Russell et al., 2004) and can be explained in terms of uranium speciation in seawater because uranium can easily form complexes with carbonate ions (Markich, 2002). Thus, the result of increase U/Ca in the primary polyp juvenile skeleton at high pCO₂ conditions comes from a decrease in seawater [${\text{CO}}_3^{2-}$] (Table 1; Figure 7B). Our results suggest the dependence of the two proxies (B/Ca and U/Ca) on seawater [${\text{CO}}_3^{2-}$] and therewith calcification rate, which is not merely related to pH or temperature. This may indicate the importance of understanding U/Ca and B/Ca incorporation in coral skeletal materials to deconvolve seawater carbonate chemistry and related equilibrium systems changes.

Author Contributions

DD and HW designed the study. HW completed the primary polyps sampling, executed the analytical research and interpretation, and served as primary author. FL, FT, and HW completed the LA-ICP-MS and LA-MC-ICP-MS analyses. DD and AT assisted in data interpretation and writing. AM completed the coral husbandry experimental setup, water measurements, and assisted in writing. ED assisted in the geochemical interpretation and collaborated on the manuscript.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The reviewer RA and handling Editor declared their shared affiliation, and the handling Editor states that the process nevertheless met the standards of a fair and objective review.

Acknowledgments

Funding for this research was supported by a fellowship to HW with funding to DD and AT from the Institute Pierre Simon Laplace (Labex L-IPSL) under Work Packages 4 and 5—IMPACTS—Project 16: Impacts of climate change (ocean acidification and warming) on corals, which is provided by The French National Research Agency, ANR (Grant no. ANR-10-LABX-0018). LA-MC-ICP-MS analysis of boron isotopes for this study was partly funded by the French National Research Agency, ANR, Project CARBORIC (Grant no. ANR-13-BS06-0013-04) to ED. AM was supported by a Marie Curie International Outgoing Fellowship (Grant Agreement # PIOF-GA-2008-235142, Project Title: AMICAL). We thank the following people and groups for their assistance: Sandrine Caquineau (IRD/LOCEAN) for Scanning Electron Microscopy analysis (ALYSES Platform, IRD/LOCEAN); Dominique Blamart (CNRS/LSCE) and Claire E. Lazareth (IRD/LOCEAN) for insightful open discussions, suggestions, and comments; Marine and Aquaculture Research Facilities Unit (MARFU) at James Cook University; the reviewers for providing constructive criticisms and helpful suggestions to improve this manuscript. This is LSCE contribution number 6105.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/article/10.3389/fmars.2017.00129/full#supplementary-material

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