Aquacult Int DOI 10.1007/s10499-017-0153-y
Effects of near-future-predicted ocean temperatures on early development and calcification of the queen conch Strombus gigas Dalila Aldana Aranda 1 & Nancy Brito Manzano 2
Received: 23 September 2016 / Accepted: 24 April 2017 # Springer International Publishing Switzerland 2017
Abstract The queen conch, Strombus (Lobatus) gigas, is one of six species of conch distributed throughout the Caribbean of significant commercial importance. The Caribbean region is adversely impacted by climate change, which affects the marine ecosystems and the calcification process of organisms with calcareous structures, such as mollusks. We tested the influence of global warming predicted in 2100 on queen conch, Strombus gigas larval development, growth, survival rate, and calcification by exposing egg masses and larvae to increased temperatures (28, 28.5, 29, 29.5, and 30 °C) for 30 days. For analysis of calcification, imaging and chemical mapping (proportion, wt) were performed on 30-day-old larvae using a highresolution scanning electron microscopy (HR-SEM) and X-ray photoelectron spectroscopy (XPS). A temperature of 30 °C resulted in the highest larval growth rate (mean ± SD 27.33 ± 2.96 μm day−1), significantly among treatments (p ≤ 0.05). Development was fastest at 30 °C, where the first larvae settled by day 27 (49%) and the mortality rate was 76%. At 28 °C, day 29 was the first day where settlement was observed for 20% of the larvae. There are significant differences among treatments on larval growth and development. The calcification process of S. gigas larvae was not affected by the experimental temperatures tested. Percent Ca content of shelled larvae showed no significant differences among treatments (mean ± SD 25.44 ± 4.74 and 24.99 ± 0.74% w for larvae grown at 30 and 28 °C, respectively). Keywords Shell calcification . Larvae development . Effect temperature . Climatic change . Mollusk Strombus
* Dalila Aldana Aranda
[email protected]
1
Laboratorio de Conservación, Cultivo y Biología de Moluscos. Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Carretera Antigua a Progreso, Km. 6, A.P. 73 Cordemex, 97310 Mérida, Yucatán, C. P, Mexico
2
División Académica de Ciencias Agropecuarias, Universidad Juárez Autónoma de Tabasco, Km 25 carretera Villahermosa-Teapa R/A La Huasteca 2ª. Sección, Villahermosa, Tabasco, Mexico
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Introduction The increase in mean sea-surface temperatures by 2100 is predicted to lie between 1.1 and 6.4 °C (The Intergovernmental Panel on Climate Change 2007), and the magnitude of estimated change differs markedly among regions. The current temperature range of the Caribbean Sea is between 24 and 30 °C, and by 2100, the mean sea-surface temperature is predicted to be between 28.7 ± 1.37 and 30.18 ± 0.57 (Smith et al. 2008; Eakin et al. 2010; Chollet et al. 2012; Agard 2014). Atmospheric CO2 concentrations increased at a rate of 1% per year in the twentieth century but are now increasing ∼3% per year and may exceed 800 ppm by the end of the current century (Caldeira and Wickett 2003; Orr et al. 2005; Porter 2007; Feely et al. 2009; Byrne et al. 2013). Climate change is modifying the distribution and productivity of marine and freshwater species and is already affecting biological processes (mass mortality, increased disease, hypoxia, coral bleaching, and species invasions) and altering food webs (Southward et al. 1995; Stachowicz et al. 2002; O’Connor et al. 2007; Coma et al. 2009; Travers et al. 2009; Sheppard et al. 2010). The consequences for sustainability of aquatic ecosystems, fisheries, and aquaculture are uncertain (Yazdi and Shakouri 2010; Hughes et al. 2003). Acidification could impede calcareous shell formation, an effect perhaps exacerbated by increased water temperature and thereby to have an impact on mollusk culture. This has received little attention and warrants urgent research. Currently, mollusk culture accounts 25% of all aquaculture and therefore any negative impacts on shell formation could significantly impact on total aquaculture production. Moreover, fisheries are a major source of inputs for aquaculture, providing feed and natural seed collection, particularly in mollusk (De Silva and Soto 2009). Early life history stages are particularly at risk, because of their sensitivity to warming temperatures, being a bottleneck for species persistence and ecological success in a changing ocean (Harley et al. 2006; Brierley and Kingsford 2009; Byrne 2011). Ocean warming reduced availability of the carbonate ions required for skeletogenesis (O’Connor et al. 2009). The thermodynamic stability of CaCO3 implies that lower pH and higher temperature values have a greater impact on more soluble polymorphs such as aragonite and high-Mg calcite (Mg/Ca >0.04) (Ries 2011; Yoshimura et al. 2011; Mavromatis et al. 2012). Moreover, Sanyal et al. (2000) and Yoshimura et al. (2015a) studied the contribution of boron to inorganic calcite, showing that changes in the relative proportions of the B/Ca ratio were incorporated into the calcite structure of Octocorallia corals. Larval mollusks show maximal growth and survival rates under ideal temperature conditions (e.g., ∼24 and 28 °C for many northwestern Atlantic and Caribbean species, respectively). Survival rate decreased at high temperature and low pH for Bathymodiolus childressi, Mytilus trossulus and Mercenaria mercenaria, and C. gigas (Zippay and Hoffmann 2010a; Arellano and Young 2011; Gazeau et al. 2011). A higher value of calcium was reported in the larvae shell of M. mercenaria reared at 28 °C than 24 °C (Talmage and Gobler 2011). Kurihara et al. (2007) observed a diminution of shell calcification for veliger larvae of C. gigas reared at 7.4 pH than those reared at 8.1 pH. The queen conch, Strombus gigas, is one of six species of conch distributed throughout the Caribbean (Berg 1976). S. gigas is a valuable mollusk of significant commercial importance in this region (Theile 2001; Aiken et al. 2006; Oxenford et al. 2008). The high market demand and lucrative export trade have resulted in heavy fishing pressure which, coupled with its vulnerable life history, has caused substantial reductions in conch populations. The Caribbean region is also adversely impacted by climate change which affects the calcification process of
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marine organisms (Orr et al. 2005). Stoner et al. (1992) and Barilé et al. (1994) reported that larvae of S. gigas are susceptible to temperature variations. Davis et al. (1993) and BritoManzano and Aldana-Aranda (2004) reported optimal growth of these larvae at 27 and 28 °C, respectively. Based on the predicted mean sea-surface temperature by 2100 in the Caribbean, the aim of our study was to determine the effect of various increased temperatures on S. gigas larvae development settlement, growth, survival, and shell calcification using energydispersive X-ray analysis (EDX) over a period of 30 days in laboratory culture.
Materials and methods Five fertilized egg masses were used for the experiment. These were collected in the Yucatan Peninsula, Mexico (22° 21′ N and 89° 49′ W). The egg masses were collected under female conch to ensure species identity and egg freshness. They were subsequently transported to the laboratory, where epibionts and sand particles were removed, and were then cleaned with filtered and UV-sterilized seawater. Egg masses were placed on a 300 μm mesh and kept immersed in a 25-L aquarium with seawater filtered through 2-μm cotton filters and UVsterilized. Larvae were reared from hatching to settlement under five temperatures (28.0, 28.5, 29.0, 29.5, and 30.0 °C) and at a pH of 8.1. A Diurnal Plant Growth Chamber (SRI21D SHEL LAB) was used to control the five temperatures and the photoperiod (12 h/12 h). There were three replicates for each trial established on an egg mass. Larvae were stocked in 10-L containers with a starting density of 100 larvae L−1. Larvae were fed equal amounts of fresh concentrates of the algae Nanochloropsis oculata at a concentration of 1000 cells ml−1 (García Santaella and Aldana Aranda 1994; Brito-Manzano et al. 1999). Every 2 days, 30 larvae were collected at random from each replicate to observe growth and development. Each day, veligers were transferred to new containers with fresh seawater filtered through 2-μm cotton filters. Larval growth was assessed by recording increments in the shell length axis. Larvae were measured using a compound microscope with a calibrated ocular micrometer to the nearest 0.10 μm. Growth rate was calculated as average growth rate in μm day−1. Differences between means were tested using ANOVA and post hoc Tukey’s tests were used to discriminate differences between all effects of temperatures examined for each ANOVA. Normality and homocedasticity of data for each indicator was checked prior to analysis using a Kolmogorov–Smirnov’s and a Levene’s test, respectively (Sokal and Rohlf 1995). The minimum significance level was set at p < 0.05. For observation of development, every day, ten larvae were collected from the batches at random from each replicate. Larvae were placed in a microscope slide to be anesthetized using a solution of 3 mM MgCl2 in sea water (Enriquez et al. 2015). Developmental characteristics of larvae were analyzed by light microscopy with examination of velum number of lobes, number of shell whorls, tentacles, and eye stalks. Settlement was determined by the reabsorption of velar lobes, outward migration of eyes, foot and operculum, and swim-crawl. According to Brito et al. (1999), developmental characteristics were numbered chronologically as they appeared and then calculating the incidence percentage in the developing larvae. Survival rates were calculated using the number of living larvae at the beginning of the experiment and at 10, 20, and 30 days of the experiment. Chemical analysis of shell calcification was performed on 30-day-old larvae. Five larvae were analyzed per temperature studied for the different temperatures studied. Larvae were fixed in 2.5% glutaraldehyde in a 0.2 M cacodylate buffer at pH 7.2 for 2 h, which was made
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isosmotic to seawater by adding sodium chloride. Samples were then rinsed with an isosmotic buffer, dehydrated through an ascending acetone series, critical-point dried and sputter-coated with gold before observation (Glauert 1975; Enriquez et al. 2015). Larvae were observed in a high-resolution scanning electron microscope (HR-SEM). Imaging and chemical mapping were carried out by using JEOL equipment, model 7600F. The chemical bonding state was investigated by XPS, carried out in Thermo Scientific equipment, model K-Alpha; XPS spectra were recorded using a scanning step of 0.1 eV for high-resolution analysis. Chemical analyses were obtained using standard sensitivity factors for our XPS equipment (Volland et al. 2012). The XPS analysis and chemical mappings were performed over the entire surface and along the shell length axis, analyzing calcium, magnesium, boron, bromine, carbon, nitrogen, and oxygen for each larval shell. For simplicity, only figures of the 28 and 30 °C treatments are presented in the results.
Results Shell development, average shell size, growth rates, and survival are shown in Table 1, for the five treatments. The ANOVA test showed significant differences on growth and survival rate. Average shell length of larvae was significantly lower at 28 and 28.5 °C with 941 ± 11.92 and 953 ± 11.81 μm, respectively. In contrast, at 30 °C growth was significantly higher with 1211 ± 22.33 μm and a daily growth rate of 27.33 ± 2.96 μm. Larvae reached four shell whorls at 23 days in 28% of the organisms reared at 30 °C and in 24% of the larvae at 28 °C. At 30 °C, larvae showed the fastest growth rate during the experiment, which was significantly higher than for the other treatments; however, survival tended to be lower. The highest survival was attained at 28 °C with 35%, which was significantly higher than larvae reared at 30 °C with 23%. Larval development characteristics are shown in Table 2. At 11 days, 58% of larvae reared at 28 °C had four lobes and three shell whorls; at 30 °C, larvae reached this stage at 9 days (54%). At 27 days of culture, 49% of larvae reared at 30 °C were competent for settlement and only 20% of the larvae demonstrated this behavior at 28 °C in 29 days. Temperature versus settlement and survival rate resulted in a high r2 (0.96 and 0.72, respectively). Figure 1a, b shows images of the elemental content analysis of larvae reared at 28 °C and Fig. 1c, d illustrates larvae reared at 30 °C and their elemental analysis (images of treatments 28.5, 29, and 29.5 °C are not presented for simplicity). It is possible to identify three peaks in larval shells located at a binding energy of 400.1 eV in all spectra. These peaks correspond to the photoemission associated with Ca bonds. The spectra of Ca along the shell length of larvae are not uniformly distributed; peaks in Ca were observed in the first and last spires. The elemental content analysis along the shell length axis of 30-day-old larvae reared at 28 and 30 °C is summarized in Table 3. The XPS showed the presence of calcium, magnesium, and boron. The percentage of calcium in larvae reared at 28 and 30 °C was similar, with 24.99 and 25.44%, respectively. However, magnesium and boron concentrations were greater in larvae reared at 28 °C than at 30 °C. Figure 2b, c, e, f shows the EDS elemental mappings for Ca and Mg, for larvae reared at 28 and 30 °C. These mappings are not uniformly distributed along the surface of shells. Shells of larvae showed zones deficient in these elements, which were denser at the apex and whorls from the spire than the body whorl or siphonal canal. As can be seen, magnesium was present in all samples; the image
1 100 1 100 1 100 1 100 1 100
4 100 4 100 3 100 3 100 3 100
7 52
8 33 8 40 7 47 746
10 49 10 38 9 42 9 55 9 54
3.0 Days % 11 58 11 59 11 100 9 54 9 41
3.5 Days % 15 31 15 37 15 38 15 45 15 53
4.0 Days % 23 24 23 25 23 29 23 35 23 38
4.5 Days %
295 ± 0.98
293 ± 2.30
303 ± 3.01
297 ± 1.89
300 ± 2.63
1211 ± 21.65 c
1189 ± 22.83 c
972 ± 11.93 b
953 ± 11.81 a
941 ± 11.92 a
Final
Initial
2.5 Days %
1.5 Days %
2.0 Days %
Shell length (μm)
Number of shell whorls
27.33 ± 2.96 c
26.66 ± 3.01 b
21.66 ± 2.72 a
22.33 ± 2.54 a
24.00 ± 3.60 a
Average growth rate (μm day−1))
Significant differences (ANOVA, Ft < 0.07, P = 0.79, n = 25) between treatments are represented with different letter in the same column
30.0 ± 0.23
29.5 ± 0.18
29.0 ± 0.03
28.5 ± 0.27
28.0 ± 0.29
Temperature (°C)
Table 1 Shell development, growth, and survival rates (average and ± SD) of larvae of Strombus gigas reared at five temperatures
23 b
24 b
23 b
36 a
35 a
Survival rate (%)
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Aquacult Int Table 2 Average of five larval cultures of Strombus gigas Developmental characteristics
2 velar lobes and 2 shell whorls 4 velar lobes and 2 shell whorls 4 velar lobes and 3 shell whorls 6 velar lobes and 3.0 shell whorls 6 velar lobes and 4.0 shell whorls Eyes on top of stalks Settlement
Temperatures (°C) 28 ± 0.29
28.5 ± 0.27
29 ± 0.03
29.5 ± 0.18
30 ± 0.23
Days
%
Days
%
Days
%
Days
%
Days
%
4 6 11 14 15 23 29
100 33 58 41 31 25 20
4 6 11 13 15 23 29
100 41 59 37 57 28 22
3 5 11 13 15 22 27
100 48 100 40 38 30 31
3 5 9 13 15 23 27
100 44 41 52 45 32 42
3 5 9 13 15 23 27
100 52 54 55 53 35 49
Percentage of larval development characteristic for each of the temperature conditions on the first day when the character appears (each developmental characteristic was of n = 150 larvae analyzed)
Fig. 1 Elemental content analysis established by scanning the shell length along a line of 30-day-old larvae, Strombus gigas (Mollusca Gastropoda) at a normal pH (8.1) at 28 °C (a, b) and 30 °C (c, d), using highresolution scanning electron microscopy (HR-SEM) and X-ray photoelectron spectroscopy (XPS). Calcium, magnesium, boron, bromine, carbon, nitrogen, and oxygen contents were determined
Aquacult Int Table 3. Average and SD of elemental content analysis established by scanning the shell length axis along a line, of 30-day-old larvae of Strombus gigas (n = 5 larvae) at pH 8.1, 28 and 30 °C, using a high-resolution scanning electron microscopy (HR-SEM) and X-ray photoelectron spectroscopy (XPS)
Ca Mg B C N O
28.0 °C Average ± SD
31.0 °C Average ± SD
24.93 ± 0.74 n.s. 0.22 ± 0.18* 2.42 ± 2.99* 22.53 ± 0.08* 7.47 ± 2.98* 41.67 ± 6.62*
25.43 ± 4.74 n.s. 0.19 ± 0.17* 0.89 ± 1.79* 26.32 ± 12.97* 3.26 ± 0.23* 47.18 ± 4.56*
Elemental content of calcium, magnesium, boron, bromine, carbon, nitrogen, and oxygen are analyzed n.s. no significant difference *Significant difference between treatments
was not as bright for larvae reared at 30 °C, where their mapping showed zones with low content of magnesium (Fig. 2f). The percentages of larval mortality showed that larvae of 1–10 days old had the highest mortality than larvae of 21–30 days old. Mortality was significantly higher for the larvae reared between 29 and 30 °C than the larvae reared between 28 and 28.5 °C (Table 4).
Discussion The present series of experiments demonstrated that optimal growth took place at 30 °C (shell length of 1211 μm); however, at this temperature, larval mortality was also highest. Davis et al.
Fig. 2 Elemental content analysis for each 30-day-old larva was established by scanning the total shell of larvae, Strombus gigas (n = 5) at pH 8.1. a Microphotography of larvae reared at 28 °C. b Calcium mapping. c Magnesium mapping. d Microphotography of larvae reared at 30 °C. e Calcium mapping. f Magnesium mapping. Elemental analysis was determined using energy-dispersive X-ray analysis (EDX) with a highresolution scanning electron microscopy (HR-SEM) and X-ray photoelectron spectroscopy (XPS)
Aquacult Int Table 4 Average percentage of larval mortality and SD for the five temperature treatments during three larval periods: P1 = 1–10-day-old larvae, P2 = 11–20-day-old larvae, P3 = 21–30-day-old larvae Larval periods Temperatures (°C)
P1 Average ± SD
P2 Average ± SD
P3 Average ± SD
28.0 28.5 29.0 29.5 30.0
37 36 42 41 45
26 35 31 27 25
2 3 4 8 7
± ± ± ± ±
0.29 0.27 0.03 0.18 0.23
± ± ± ± ±
1.41 0.83 0.54 1.30 1.67
± ± ± ± ±
8.87 7.90 9.97 8.91 8.11
± ± ± ± ±
6.30 6.70 1.40 8.01 7.47
(1993) cited an optimal temperature for growth of 27 °C for S. gigas larvae, while García Santaella and Aldana Aranda (1994) and Brito Manzano (2004) noted optimal development at 28 °C. In relation to the larval development of S. gigas, Brownell (1977) observed metamorphosis between 28 and 33 days, Sidall (1983) and Hensen (1983) from 20 to 28 days, while Ray and Davis (1989) observed this characteristic between 21 and 40 days. In this study, metamorphosis took from 27 to 29 days, recorded in 49 and 20% of the larvae reared at 30 and 28 °C, respectively. The greatest mortality in coral, mollusk, and sea urchin embryos occurs prior to or at gastrulation as a response to thermal challenge (Kinne 1970; Byrne et al. 2009; Randall and Szmant 2009). Effect of temperature has been studied in larvae of different species of mollusks (Schetelma 1967; Zippay and Hofmann 2010a, b). These authors observed a direct effect on the survival rate of Haliotis sp. and Nucella ostrina, with an increase in mortality from 40 to 80% at higher temperatures. Results on survival obtained by different authors with S. gigas larvae reported a survival between 6 and 17% (Hensen 1983), while Heyman et al. (1989) and Davis et al. (1993) reported 59–60%, respectively. In this study, survival varied from 23 to 35%; with the best results obtained at 28 °C. We also observed a more marked effect of temperature on the early stages of larvae than those close to settlement (Table 3). Similar results were presented by Wright et al. (1983) and Byrne et al. (2009) in early development (trochophore stage) in the bivalve Argopecten irradians, where this stage was observed to be more vulnerable to increasing temperatures than later larval stages. Furthermore, water viscosity is inversely related to temperature. This simple physical relationship couples two potential influences on organism performance. Podolsky (1994) manipulated seawater viscosity, with and without temperature, to distinguish the physiological and mechanical effects of temperature on suspension feeding by ciliated echinoderm larvae. This author showed that change in viscosity alone accounted for half of the decline in the feeding rate at the lower temperature. High viscosity shifted ingestion toward larger particles, which suggests that viscosity affects particle capture as well as rates of water processing. Temperature impacts suspension feeding independently of physiology and has implications for many small-scale biological processes, where viscous forces dominate motion. Cilia and flagella are used to generate feeding currents and to capture particles, processes that may both be sensitive to temperature-induced viscosity change (Jorgensen 1983; Shimeta and Jumars 1991). In this study, the effect of increased seawater viscosity at a higher temperature could explain the higher mortality obtained for early larvae (1–10 days old) than 20–30-day-old larvae (Table 3).
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Elevations in both CO2 and temperature synergistically reduced the calcification rate of scleractinian corals (Reynaud et al. 2003). On the other hand, Zeebe and Wolf-Gladrow (2001) reported CaCO3 to be more soluble at lower temperatures. Further comparison of CO2 sensitivity is needed for marine organisms from different latitudes. Byrne et al. (2011) observed the effect of ocean acidification on larval development with abalone (Haliotis coccoradiata) at 20, 22, and 24 °C and pH levels of 8.1, 7.8, and 7.6, and reported a greater percentage of calcified larvae at lower temperatures (20 °C, 60% and normal pH). For sea urchin larvae, Byrne et al. (2013) reported that Ca was higher at a high temperature and a pH of 8.1 than at a low pH (7.6) and high temperature. In contrast, Talmage and Gobler (2011), compared the responses of three species of calcifying bivalves (M. mercenaria, C. virginica, and A. irradians) observing that increases in temperature and CO2 reduced survival, development, growth, and lipid synthesis of larvae. These authors reported increases in calcium with temperature regardless of the pH level. Miller et al. (2009) observed that the amount of CaCO3 biomineralized by Crassostrea virginica larvae decreased as pCO2 increased while C. ariakensis showed no change to either growth or calcification. Both species demonstrated net calcification and growth, even when aragonite was under saturated, a result that runs counter to previous expectations for invertebrate larvae that produce aragonite shells. In relation to warming and acidification effects on calcification mollusk larvae, most authors measure the degree of calcification indirectly, by dissolving the shell and determining the amount of calcium by inductively coupled plasma/optical emission spectroscopy. In this study, we directly determined the amount of calcium in the shells of larvae, using backscattering electron (BSE) imaging and chemical analysis by XPS spectra. These analyses showed that calcium was similar in the shell of larvae reared at 30 and 28 °C; however, magnesium and boron concentrations were greater in larvae reared at 28 °C than at 30 °C. Though the bulk of the shell mineral is calcium carbonate (either aragonite or calcite), other environmental elements are often incorporated, for example, boron, magnesium, strontium, and sulfur during mineralization (Rosenberg and Jones 1975; Furst et al. 1976). Foraminifera, corals, Gastropoda, and Pelecypoda yield large variations in boron concentration that range from 1 ppm in gastropod shells to 80 ppm in corals. The boron content of the biogenic calcareous skeletons is independent of mineralogical composition and is probably related to biological effects. Carbonates are an important sink for boron in the oceans (Vengosh et al. 1991). Boron geochemistry in carbonate materials have revealed that boron is enriched in aragonite (15 ppm) relative to that in calcite (9 ppm) and that boron is concentrated in the nonorganic parts of the shell matrices of bivalve mollusks (Roopnarine et al. 1998). Borate boron concentrations in seawater do not vary with temperature, but rather only with salinity. Nevertheless, it is possible that the coefficient of incorporation into aragonite could be temperature dependent (Roopnarine et al. 1998). In this study, we observed less boron in the shells of larvae reared at 30 °C than those reared at 28 °C. Chavez (personal communication) observed less aragonite in the shells of larvae reared at 28 °C than those reared at 31 °C. Yoshimura et al. (2015a) investigated B, Ba, and U element partitioning in the calcite skeletons of Octocorallia corals collected at a range of water depths; B/Ca exhibited a clear increasing trend with depth. These authors also observed a higher B/Ca and Ba/Ca along the central axis of the skeleton of the semi-fossilized C. elatius, compared to their values in more marginal samples; furthermore, clear growth bands were apparent along the growth axis. In this study, analyses performed along the shell length axis showed higher boron content in the first spire of the shell larvae, compared with values in the siphon canal and the outer lip (Fig. 1a–d) for both temperatures.
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In the coral samples, the Mg/Ca ratio showed a clear positive correlation with water temperature (Tarutani et al. 1969; Yoshimura et al. 2011; Mavromatis et al. 2012; Yoshimura et al. 2015b). Octocorallia (Anthozoa) coral skeletons are composed of high-Mg calcite (Sherwood et al. 2005). Three polymorphs of CaCO3 have different solubility in seawater and the thermodynamic stability of CaCO3 implies that lower pH and higher temperature values have a greater impact on more soluble polymorphs such as aragonite and high-Mg calcite (Ries 2011). In this study, shells of larvae reared at 30 °C showed less Mg than shells of larvae reared at 30 °C. Findings in this study suggest that current and future increases in temperature in the Caribbean Sea are likely to have a negative effect on survival rates of S. gigas larvae. Nevertheless, calcification of larvae was not affected by the influence of global warming predicted in 2100. In contrast, larval mortality was affected by elevated temperature. Based on these results, it would be interesting to test the effect of temperature and ocean acidification on the calcification process throughout the larval life stage for this endemic mollusk from the Caribbean Sea. Acknowledgements This study was supported by the proposal of Mexicain Council for Science, CONACyT No. 181329 (El caracol rosa como indicador del cambio climático en el Caribe: Calentamiento y Acidificación oceánica). Measurements were performed at LANNBIO CINVESTAV IPN Merida (Lab-2009-01 No. 123913, CB2012/178947). The authors acknowledge Dora Huerta for technical support on electron microscopy and Dr. Gemma Franklin, a native English speaker, for reviewing the manuscript. The authors are grateful for the comments made by the two reviewers to improve this work.
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