The carbonate system on the coral patches and rocky intertidal habitats of the northern Persian Gulf: Implications for ocean acidification studies

Marine Pollution Bulletin 151 (2020) 110834

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The carbonate system on the coral patches and rocky intertidal habitats of the northern Persian Gulf: Implications for ocean acidification studies

T

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Abolfazl Saleha, , Jahangir Vajed Samieib, Fatemeh Amini-Yektaa, Mehri Seyed Hashtroudia, Chen-Tung Arthur Chenc, Neda Sheijooni Fumania a

Iranian National Institute for Oceanography and Atmospheric Science, No. 3, Etemadzadeh St., Fatemi Ave., Tehran 1411813389, Iran Department of Marine Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany c Department of Oceanography, National Sun Yat-sen University, Kaohsiung 80424, Taiwan, ROC b

A R T I C LE I N FO

A B S T R A C T

Keywords: Carbonate chemistry Persian Gulf Rock pools Intertidal rocky shore Coral Ocean acidification

This research characterizes the temporal and spatial variability of the seawater carbonate chemistry on the nearshore waters of the northern Persian Gulf and Makran Sea. In general, normalized total alkalinity (nAT) showed a westward decrease along the coasts of Makran Sea and the Persian Gulf. Intertidal seawater was always supersaturated in terms of calcium carbonate minerals during the daytime. Rocky shore waters in the Persian Gulf were sinks for CO2 in the winter during the daytime. The nAT decreased from Larak to Khargu Island by 81 μmol/ kg. As expected, the two hypothetical drivers of bio-calcification, i.e., Ω and the [HCO3−]/[H+] ratio, were significantly related at a narrow range of ambient temperature. However, as data were pooled over seasons and study sites, in contrast to ΩAr, the [HCO3−]/[H+] ratio showed a slight dependence on temperature, suggesting that the ratio should be investigated as a more reliable factor in future biocalcification researches.

1. Introduction On global and regional scales, the inorganic carbon chemistry (and the acidity) of the ocean is changing due to the anthropogenic increase of the atmospheric concentration of carbon dioxide (CO2). Ocean acidification (OA) might impact many biological processes including the pH balance, metabolism, and calcification with possible consequences for growth, development, and survival of many marine pelagic (Iglesias-Rodriguez et al., 2008; Riebesell and T.P.D., 2011) and benthic organisms (Gazeau et al., 2013; Kleypas and Langdon, 2006; Kroeker et al., 2013; Langdon et al., 2003; Orr et al., 2005). Calcifying organisms are especially sensitive to OA as they rely heavily on the carbonate saturation state (Ω; Langdon et al., 2003) or on the bicarbonate to hydrogen ion concentration ratio (SIR; Bach, 2015) to form their skeletons, shells, and other structures. Near-shore areas are highly variable environments due to processes which change local inorganic carbon chemistry, such as enhanced biological activities and physical transportation of high CO2 waters from sub-thermocline layers. Both the OSPAR/ICES Study Group on Ocean Acidification (SGOA, ICES 2014) and the Global Ocean Acidification Observing Network (GOA-ON, Newton et al., 2015) identified particular gaps in carbonate data for coastal and inshore waters (León

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et al., 2018). This gap in knowledge has raised questions regarding potential consequences of OA for near-shore ecosystems. To be able to accurately predict future impacts of OA on marine organisms in nearshore coastal environments, it is necessary to understand the present conditions and the variability of seawater carbonate chemistry in these environments. The Persian Gulf is a shallow, sub-tropical sea adjacent to the northwestern Indian Ocean (Michael Reynolds, 1993). It harbors some of the shallow-water coral assemblages (Bento et al., 2016; Riegl and Purkis, 2012; Sheppard et al., 2010), which are already affected by extreme environmental conditions and substantial seasonal variation in temperature, irradiance, and seawater inorganic carbon chemistry (Kleypas et al., 1999; Vajed Samiei et al., 2015, 2016; Vaughan and Burt, 2016). Majority of hard corals in the Gulf do not build reefal frameworks (Riegl and Purkis, 2012). Therefore, changes in water chemistry may impacts these fragile non-reefal frameworks which they rely upon for colonization over the next 50 years (Purkis et al., 2011). There are a few studies addressing changes in the calcification rates of some coral species under the influence of declining pH (lab-based experiments) (Behbehani et al., 2019) or seasonal variation of the calcium carbonate saturation state (Ω) in the field (Vajed Samiei et al., 2016). However, there is still no published information on the full

Corresponding author. E-mail addresses: [email protected] (A. Saleh), [email protected] (C.-T.A. Chen).

https://doi.org/10.1016/j.marpolbul.2019.110834 Received 11 September 2019; Received in revised form 7 December 2019; Accepted 15 December 2019 Available online 29 January 2020 0025-326X/ © 2019 Elsevier Ltd. All rights reserved.

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nearshore areas) and coral patches of the eastern- and northern-most Islands in the Persian Gulf during the period of 2014 to 2016 (Table 1 and Figs. 1 and 2). In each season, measurements of parameters including pHNBS, temperature, dissolved oxygen (DO) and salinity at different locations were performed using a HACH portable meter HQ40d over two to four consecutive days around midday (10:00–14:00). In the case of rock pools, all measurements and water samples were taken at the end of the emersion period, just before they were again covered by the tide. Seawater pH and temperature measurements were performed using a combined glass/reference electrode (HACH, IntelliCAL PHC101) calibrated by NBS buffers (accuracy of ± 0.02, precision of ± 0.001). Salinity was determined using a conductivity probe (HACH, IntelliCAL CDC401 with the precision of ± 0.1) calibrated by a certified reference seawater. Dissolved oxygen was measured using a calibrated dissolved oxygen optical sensor (HACH, IntelliCAL LDO101 luminescent/optical dissolved oxygen probe). During summer (14th Aug. to 3rd Sep. 2015) and winter (16th Jan. to 8th Feb. 2016), measurements and sampling were made at the same positions and depths in each rock pool after seawater was homogenized. In the case of coral patches, all onboard measurements and sub-samplings were performed on water samples taken from a depth of 1 m above corals using a 4-L Niskin water sampler. Water samples for determining dissolved inorganic nutrients were immediately filtered by syringe filters (0.45 μm, cellulose acetate), collected in 125 mL high-density polyethylene bottles and quickly frozen until further analysis (Grasshoff and Ehrhardt, 1999). Water samples for determining total alkalinity (AT) were collected in 500 mL glass bottles and 100 μL of a saturated mercury(II) chloride (HgCl2) solution were added to stop the biological activities (Dickson et al., 2007). Samples were stored at 4 °C until laboratory analysis. Dissolved inorganic nutrients were determined using spectrophotometric techniques (ROPME, 1999) with a UV–Vis spectrophotometer (Analytikjena, Specord 210). Repeatability (relative standard deviation) for determination of phosphate and silicate in seawater were better than 5 and 10%, respectively. AT was determined by potentiometric open-cell titration (Dickson et al., 2007, SOP03b) using a digital 715 Dosimat titrator (Hydro-bios). Non-linear least-squares fitting of titration data at the pH range of 3.0 to 3.5 were used to calculate AT. The precision of AT measurements was determined to be better than ± 3.5 μmol/ kg (0.15%) by titrating 10 subsamples of a secondary standard of seawater collected from the Strait of Hormuz to monitor the reproducibility of the system. The accuracy of the AT measurements was evaluated by analyzing certified reference materials (CRM, batch#182, A.G. Dickson, Scripps Institution of Oceanography, La Jolla, CA, USA). Carbonate chemistry of seawater was characterized based on pHNBS, AT, temperature and salinity (and dissolved phosphate and silicate where they were measured), the CO2SYS software version 2.3 (Pierrot and Wallace, 2006), and stoichiometric dissociation constants defined by Mehrbach et al. (1973) and refit by Dickson and Millero (1987).

characterization of carbonate chemistry of seawater on the coral patches of the Persian Gulf while being one of the critical research needs for identifying future changes in the Persian Gulf coral reef ecosystems (Feary et al., 2013). Rocky intertidal shores in the northern Persian Gulf and Makran Sea (north of the Oman Sea) are among the richest habitats with considerable biodiversity in the region due to the topological complexity and various microhabitats (Amini-Yekta et al., 2019). Rocky shores have a high abundance of diverse microflora and microfauna, especially in temperate zones (Webber and Thurman, 1991). Organisms living in intertidal shores are exposed to consecutive periods of immersion and emersion. During low tides, organisms undergo harsh environmental conditions characterized by high temperature and salinity variations, higher solar radiation and dryness (Martinez et al., 2012; Tomanek and Helmuth, 2002). Organisms experiencing such harsh conditions can find refuge in intertidal rock pools which are filled with seawater during high tide but exist as separate pools at low tide (Amini-Yekta et al., 2019; Daryanavard et al., 2015; Legrand et al., 2018a). However, variations in physical and chemical properties of seawater in rock pools remain much greater than those of subtidal habitats (Legrand et al., 2018b; Morris and Taylor, 1983). There are several studies reporting the diurnal and seasonal variations of temperature, oxygen concentration, pH and salinity in rock pools, including one in the rocky shores of Qeshm Island, Persian Gulf (Daryanavard et al., 2015; Metaxas and Scheibling, 1993; Morris and Taylor, 1983). However, there are a few studies in which carbonate chemistry of seawater has been determined in rock pools (Egilsdottir et al., 2016; Legrand et al., 2018b; Truchot and Duhamel-Jouve, 1980; Williamson et al., 2014, 2017). The most recent ecological characterization study including inorganic carbon chemistry within intertidal rock pools was performed by Legrand et al. (2018a, 2018b) on the north-western coast of Brittany, France, in which, rock pools have been characterized in terms of the complex interactions among physical and chemical parameters with biological processes. Considering the lack of baseline ocean acidification information in the Persian Gulf, the objective of this article is to report the results of our recent studies on the spatial and, in some locations, temporal variability of carbonate chemistry in the easternmost and northernmost coral patches and rocky intertidal shores of the Persian Gulf together with two locations in Chabahar bay and Makran Sea coasts (located in northeast Oman Sea). The results reported herein address some of the gaps in the current understanding of carbonate chemistry and act as a starting point for further studies aiming to better understand these valuable habitats which are of major economic, ecologic, scientific, and social importance.

2. Methods Inorganic carbon chemistry of seawater was studied in nine different locations in the northern Persian Gulf and Makran Sea (northern Oman Sea) including rocky intertidal habitats (tidal pools and Table 1 Sampling and measuring locations in the Persian Gulf and Makran Sea. Habitat type

Region

Site name

Coordinates

Coral reef

Persian Gulf

Intertidal rocky shore

Persian Gulf

Hengam Larak 1 Larak 2 Khargu 1 Khargu 2 OLI AFT MHT LIP DBG

26.659 26.878 26.822 29.299 29.332 27.833 26.751 26.786 25.320 25.277

Chabahar Bay Makran Sea

2

N; N; N; N; N; N; N; N; N; N;

55.915 56.338 56.339 50.327 50.357 51.903 54.035 55.327 60.620 60.666

Duration of study E E E E E E E E E E

Mar. 2014 to Jan. 2015 Sep. 2016 Sep. 2016 Sep. 2016 Sep. 2016 Aug. 2015, Jan. 2016 Aug. 2015, Jan. 2016 Aug. 2015, Jan. 2016 Aug. 2015, Feb. 2016 Sep. 2015, Feb. 2016

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Fig. 1. The study sites located across the northern Persian Gulf and Makran Sea.

3. Results and discussion

shore which is the innermost site. Nearshore water salinity in winter was in the range of 36.9 to 39.6 from east to west. In summer, maximum average salinity of nearshore seawater was recorded in MHT (39.8) decreasing to the value of 37.0 in DBG. Water salinity in rock pools showed a positive deviation from the corresponding values of nearshore seawater in the range of near-zero to +2.2. Daytime dissolved oxygen (DO) in nearshore seawater was in the range of 6.30 to 8.52 mg/L, and 7.26 to 9.29 mg/L in summer and winter, respectively. At the same time, the concentration of DO increased to 20.4 mg/L (388%) in summer and to 20.7 mg/L (323%) in winter in a rock pool in AFT intertidal rocky shore due to photosynthetic activities (Fig. 3b). The lowest and highest average values of pH were recorded in rock pools of MHT (8.00) and AFT (9.0) in summer and winter, respectively (for individual rock pools: 7.9 to 9.3). At the MHT the sampling time (duration of low tide) in summer was early in the morning, where respiration effects on the pH are still dominant comparing to the influence of photosynthesis. This is the reason for obtaining lowest values of pH in rock pools of this area in summer (even lower than their corresponding nearshore values). Average nearshore seawater pH was in the ranges of 8.25 to 8.40 in winter and 8.10 to 8.55 in summer. Fig. 4 demonstrates the carbonate chemistry parameters of the intertidal rocky shores of the northern Persian Gulf and Makran Sea in

Data of carbonate chemistry and related parameters for all locations and periods are summarized in Table 2. 3.1. Intertidal rocky shores Fig. 3 shows the average temperature, salinity, dissolved oxygen and in situ pH in nearshore seawater and rock pools of selected intertidal rocky shores in summer and winter. Data are related to measurements and samplings which were made at the end of the emersion period. In summer, the maximum temperature of nearshore seawater was recorded at the OLI intertidal rocky shore, 37.7 °C (the innermost intertidal site) decreasing to the value of 30.6 °C in DBG located on the Makran Sea coast (outermost site). Seawater temperature in rock pools was in the range of 31.3 to 41.5 °C in summer. Maximum temperature deviation of rock pools from nearshore seawater in summer was 5.6 °C at the AFT (Fig. 3a). In winter, nearshore seawater temperature was in the range of 22.2 to 24.7C with no longitude-dependent trend. Rock pools in LIP station showed the highest temperature deviation from their nearshore seawater (+5.0 °C). The maximum seasonal temperature variation in nearshore seawater was 14.4 °C in OLI rocky intertidal 3

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Fig. 2. Exemplary photographs of different sampling sites. a) Typical rock pools in Chabahar bay (LIP), b) intertidal rocky shore of Makran Sea coast (DBG), c) a rock pool in the Persian Gulf (MHT), d) OLI intertidal rocky shore in the Persian Gulf, e) AFT intertidal rocky shore in the Persian Gulf, f) Eastern Hengam island, g) Khargu corals, h) Larak corals. (Photos a–e by F. Amini-Yekta and f–h by J. Vajed Samiei).

average concentration in nearshore water was found to be in the range of 1094 ± 104 (OLI, August) to 1853 ± 2 μmol/kg (LIP, February). The minimum concentration of bicarbonate calculated was from rock pools of AFT in August (393.1 μmol/kg). The average carbonate concentration was in the range of 228 ± 2 (LIP, February) to 491 ± 30 μmol/kg (OLI, August) in nearshore seawater samples. The maximum average concentration of carbonate calculated for rock pools of AFT in August (515.1 μmol/kg) with the highest average temperature and pH. Daytime partial pressure of carbon dioxide (pCO2) in nearshore seawater was in the range of 122 ± 28 (OLI, August) to 533 ± 5 μatm (MHT, August). Daytime data show that rocky shores at the OLI station are sink for CO2 in both winter and summer. All of the rocky shores in the PG are potential sinks for CO2 in winter daytime due to photosynthetic activities (of perhaps, mostly coralline algae) and reduced temperature. During August, rock pools in AFT showed the minimum pCO2 (average of 17.4 μatm) among all locations and seasons. The highest aragonite and calcite saturation states (ΩAr and ΩCa) in nearshore intertidal waters were calculated for OLI in summer with the average values of 8.0 ± 0.05 and 11.6 ± 0.7, respectively. Results showed that in daytime, seawater of the intertidal area was always supersaturated in term of calcium carbonate minerals with the minimum average values of 3.57 ± 0.02 and 5.42 ± 0.03 for ΩAr and ΩCa, respectively. The maximum ΩAr and ΩCa (8.59 and 12.19) were

warm and cold seasons. The average total alkalinity (AT) was in the range of 2343 ± 11 to 2463 ± 54 μmol/kg in nearshore seawater samples, increasing from DBG to OLI with a positive correlation with water salinity. Compared to nearshore water, rock pools showed reduced alkalinity (during daytime) due to biotic/chemical precipitation of calcium carbonate. Maximum reduction of total alkalinity (−709 μmol/kg) in rock pools was observed in MHT during wintertime sampling. On the other hand, trends of normalized total alkalinity (to S = 35) clearly show that nearshore seawater loses its total alkalinity in a constant salinity westward along the Makran Sea and the Persian Gulf coasts in both seasons. On average, normalized total alkalinity decreased 125 and 185 μmol/kg from DBG to OLI in winter and summer, respectively. Such a reduction has been reported before in offshore seawater of the Persian Gulf (Brewer and Dyrssen, 1985). Brewer and Dyrssen (1985) showed that on average, Persian Gulf waters have lost about 125 μeq/kg or been stripped of 62.5 μmol/kg of CaCO3 when compared to Indian Ocean surface waters of equivalent salinity. They predicted that at the coastal areas much stronger signals could be observed. The average total dissolved carbon dioxide (TCO2) was in the range of 1588 ± 75 (OLI, August) to 2093 ± 4 (LIP, February) μmol/ kg in nearshore seawater samples. Maximum reduction of TCO2 (−1028 μmol/kg) in rock pools was observed at the MHT in January due to both calcification and photosynthetic activities. Bicarbonate 4

September 2016 August 2015 January 2016 August 2015 January 2016 August 2015 January 2016 August 2015 January 2016 August 2015 January 2016 August 2015 January 2016 March 2014 June 2014 August 2014 October 2014 January 2015 September 2016 August 2015 February 2016 August 2015 February 2016 September 2015 February 2016 February 2016

Khargu coral reef OLI near shore

5

DBG rock pools

DBG near shore

LIP rock pools

Larak coral reef LIP near shore

Hengam coral reef

MHT rock pools

MHT near shore

AFT rock pools

AFT near shore

OLI rock pools

Time

Location

33.5 37.7 23.3 39.3 26.1 36.5 24.4 40.6 27.5 32.6 22.2 32.5 21.8 23.8 30.6 32 31.4 22.8 32.0 32.8 24.6 33.8 28.5 30.6 23.6 26.2

0.2 0.4 0.1 0.6 0.1 0.5 1.9

± ± ± ± ± ± ±

± 0.1

0.7 0.5 0.1 0.9 1.0 0.8 0.5 0.9 0.9 0.6 0.6 0.4 0.7 0.4 0.5

± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

Temperature (°C)

39.6 39.7 39.6 40.7 40.0 38.4 38.1 40.0 39.3 39.8 37.5 39.9 38.2 37.1 38.1 37.6 37.2 37.3 37.6 37.1 37.0 37.3 37.5 37.0 36.9 37.4

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

Salinity

0.1 0.2 0.1 0.6 0.2 0.0 0.1 0.5 1 0.5 0.3 0.2 0.7 0.2 0.4 0.1 0.2 0.1 0.1 0.1 0.1 0.1 0.5

8.20 ± 0.03 8.55 ± 0.06 8.40 ± 0.06 8.91 ± 0.15 8.66 ± 0.07 8.17 ± 0.04 8.35 ± 0.02 9.0 ± 0.4 8.7 ± 0.2 8.10 ± 0.01 8.32 ± 0.03 8.00 ± 0.14 8.9 ± 0.4 8.18 ± 0.05 8.17 ± 0.02 8.23 ± 0.03 8.15 ± 0.02 8.17 ± 0.02 8.20 ± 0.01 8.35 ± 0.02 8.19 ± 0.0 8.48 ± 0.07 8.50 ± 0.12 8.25 8.26 ± 0.6 8.50

pH (NBS)

2500 2354 2463 1963 2225 2461 2454 1942 1986 2425 2343 2430 1634 2411 2481 2460 2449 2424 2463 2423 2417 2316 2337 2425 2413 3 8 2 5 3 3 1 6

± 8

± ± ± ± ± ± ± ±

± 45 ± 11

± 13

± 30 ± 18 ± 54

AT (μmol/kg)

2054 ± 1588 ± 1965 ± 1021.6 1428.1 2007.4 2008 ± 908.6 1375.6 2068 ± 1956 ± 1971.7 927. 8 2094 ± 2099 ± 2031 ± 2085 ± 2122 ± 2054.5 1899 ± 2093 ± 1741.2 1729.5 2002.5 2055 ± 49

25 4

32 19 22 16 17

25 41

28

23 75 2

TCO2 (μmol/kg)

409 ± 122 ± 216 ± 28.9 55.2 424.2 261 ± 17.4 92.0 533 ± 271 ± 351.9 19.9 419 ± 446 ± 378 ± 473 ± 434 ± 410 ± 258 ± 412 ± 192.9 148.5 352.7 343 ± 64

59 25 32 25 32 10 18 1

5 29

14

36 28 32

pCO2 (μatm)

1735 ± 1094 ± 1622 ± 516.8 928.7 1684.2 1694 ± 393.1 1005.9 1808 ± 1684 ± 1651.4 545.4 1859 ± 1820 ± 1723 ± 1817 ± 1896 ± 1758 ± 1535 ± 1853 ± 1355.2 1321.9 1701.0 1795 ± 73

51 27 33 24 26 8 40 2

12 58

36

29 104 34

HCO3− (μmol/kg)

Table 2 Inorganic carbon chemistry of seawater in some coral patches and rocky intertidal sites across the northern Persian Gulf and Makran Sea.

309 ± 491 ± 337 ± 504.3 497.9 314.2 306 ± 515.1 367.3 248 ± 264 ± 312.2 381.9 223 ± 268 ± 299 ± 257 ± 213 ± 286 ± 358 ± 228 ± 381.6 404.0 292.8 250 ± 26

21 9 12 9 10 4 15 2

14 18

9

16 30 36

CO32− (μmol/ kg) 7.2 ± 0.4 11.6 ± 0.7 7.8 ± 0.8 11.90 11.48 7.51 7.2 ± 0.2 12.19 8.42 5.8 ± 0.3 6.2 ± 0.4 7.29 8.95 5.3 ± 0.5 6.3 ± 0.2 7.1 ± 0.3 6.1 ± 0.2 5.0 ± 0.2 6.8 ± 0.1 8.5 ± 0.4 5.42 ± 0.03 9.09 9.60 6.96 5.9 ± 0.6

ΩCa

4.9 ± 0.3 8.0 ± 0.5 5.1 ± 0.5 8.33 7.64 5.19 4.7 ± 0.2 8.59 5.61 3.9 ± 0.2 4.1 ± 0.3 4.95 5.87 3.5 ± 0.3 4.3 ± 0.2 4.8 ± 0.2 4.1 ± 0.1 3.3 ± 0.2 4.6 ± 0.1 5.8 ± 0.3 3.57 ± 0.02 6.19 6.44 4.69 3.9 ± 0.4

ΩAr

0.279 0.392 0.412 0.374 0.544 0.263 0.376 0.365 0.386 0.229 0.351 0.289 0.499 0.284 0.272 0.293 0.259 0.279 0.281 0.343 0.287 0.360 0.428 0.301 0.324

0.026 0.009 0.012 0.007 0.013 0.004 0.008 0.001

± 0.034

± ± ± ± ± ± ± ±

± 0.006 ± 0.016

± 0.006

± 0.018 ± 0.020 ± 0.044

[HCO3−]/[H+] (mol/ μmol)

A. Saleh, et al.

Marine Pollution Bulletin 151 (2020) 110834

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Fig. 3. Temperature, salinity, dissolved oxygen, and pH in rock pools and nearshore seawater of the study locations. Dashed lines: nearshore seawater; bars: rock pools; yellow color: summer, 2015; blue color: winter, 2016. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

the Persian Gulf (Brewer and Dyrssen, 1985). Therefore, it was not surprising that in seawater of Hengam coral patches (located in the Strait of Hormuz) the annual average of pCO2 obtained to be higher than atmospheric values. Calcite and aragonite saturation states were calculated to be in the range of 5.0 to 7.1 and 3.3 to 4.8, respectively. The maximum Ω for calcium carbonate minerals were recorded in August and the minimum values were found in January showing the key role of temperature on the seasonal variation of the saturation state in this area (N = 10, Pearson correlation = 0.958, sig. 0.000). Fig. 5 shows the 24-h variations of some physical and chemical properties of seawater in Hengam coral patch in a winter and a summer day. The daily variation of temperature, dissolved oxygen pH, estimated ΩAr and pCO2 were found to be 1.2 °C, 1.4 mg/L, 0.06, 0.4 and 71 μatm in September and 0.7 °C, 1.4 mg/L, 0.06, 0.5 and 80 μatm in January. The maximum effect of photosynthetic activities on the carbonate chemistry of seawater was observed at 14:30 and 14:00 in September (2012) and January (2013), respectively. Considering the atmospheric concentration of CO2 (≈393 ppm in 2012–2013), it can be seen that seawater in Hengam coral patch was a potential source of CO2 to the atmosphere except during midday when the photosynthetic activity decreased the partial pressure of CO2 in seawater. Table 3 compares the seawater carbonate parameters in the coral patch of eastern Hengam Island with those of Davies reef in the central

calculated for rock pools of AFT in August with the highest average values of temperature, pH and dissolved oxygen, due to the highest photosynthetic activity. 3.2. Coral reefs Average measured temperature of seawater in Hengam coral reefs located at the western part of the Strait of Hormuz variated between 22.8 and 32 °C from January to August (hurly logged data between 20.3 and 34.8 °C). Intra-annual variation of salinity was from 37.1 to 38.1 with the minimum and maximum values in March and June, respectively. Maximum daytime pH of 8.23 ± 0.03 was recorded in August due to a phytoplankton bloom. AT was found to be in the range of 2411 ± 3 to 2481 ± 8 μmol/kg, positively correlated with water salinity. pCO2 was obtained to be in the range of 378 ± 32 to 473 ± 25 μatm with an annual average of 430 μatm which is significantly higher than the corresponding atmospheric values (about 400–410 ppm at the time of this study). Brewer and Dyrssen (1985) have reported high-pCO2 surface water (30 μatm higher than atmospheric levels) from the Oman Sea entering the Persian Gulf through the Strait of Hormuz. Reduced temperature (in winter) and biological productivity could potentially lower pCO2 to the values even lower than atmospheric levels, as the water flows to the north and inner parts of 6

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Fig. 4. Carbonate chemistry parameters in intertidal rocky shores of the Persian Gulf and Makran Sea. Dashed lines: nearshore seawater; bars: rock pools; yellow color: summer, 2015; blue color: winter, 2016. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

shores and also studied coral patches. Biogeochemical processes such as photosynthesis, respiration, calcium carbonate precipitation, and dissolution have predictable effects on the AT and TCO2. Vectors in Fig. 6 indicate the theoretical effects of photosynthesis and calcification on AT and TCO2. During photosynthesis, CO2 is removed from the water column which reduces TCO2 by 1 mol per mol CO2, while respiration has an opposite effect. Marine plankton photosynthesis, however, slightly increases the total alkalinity of the seawater by the value of 17 units per every 106 mol of CO2 removal (Chen and Pytkowicz, 1982). Therefore, photosynthesis (plankton productivity) reduces TCO2 and increases AT by a stoichiometric ratio of 6.24:1, while the decomposition of organic matter (respiration) will have a reverse effect. On the other hand, biotic calcification and chemical precipitation of calcium carbonate result in a decrease in TCO2 and AT of seawater with a stoichiometric ratio of 1:2, whereas dissolution of calcium carbonate increases these parameters with the mentioned stoichiometric ratio (Wolf-Gladrow et al., 2007). Because photosynthesis–respiration (ncp) and calcification–dissolution (ncc) affect AT and TCO2 differently, the slope of the nAT-nTCO2 relationship indicates the balance between these two processes (i.e., the ncp:ncc ratio). The ncp:ncc ratio is given by (2/m)−1 (ignoring the effect of photosynthesis on AT and the CO2 exchange), where m is the slope of the nAT-nTCO2 line (Albright et al., 2013). This ratio was calculated to be 1.35, 2.13 and 4.35 for coral reefs, nearshore seawater, and rock pools, respectively, indicating the higher contribution of photosynthesis-respiration (rather than calcification-dissolution) in spatial variation of carbonate chemistry of seawater in studied coastal areas. Marine organisms precipitate a large amount of carbon as calcium

Great Barrier Reef (GBR), Australia (Albright et al., 2013). Seawater of Hengam corals, in a semi-enclosed water body of the PG, shows significantly higher seasonal temperature variations, salinity, total alkalinity and saturation state of aragonite. Comparison of normalized AT (nAT) between two sites clearly shows that in Hengam Island, coral community calcification could not change the chemistry of seawater significantly while, significant reduction of nAT in Davies reef shows the considerable impact of coral reef calcification on the overlaying seawater. Probably, the extent of the area covered by coral reefs and sea currents are the most important determinants of this difference. When considering Ω as an indicator of calcification, this comparison simply shows that in terms of carbonate chemistry, Hengam Island is comparable and even more favorable for calcification of coral communities than the GBR. Carbonate parameters of seawater also were determined on the coral patches of Khargu (the innermost coral site) and Larak (the outer most coral site) Islands in the PG in September 2016 (see Table 2). Values obtained on the Larak coral reef were almost similar to those of the Hengam coral reef in the summertime due to their proximity (distance of 46 km, see Fig. 1). Seawater on the coral reef of Khargu Island showed higher salinity, summertime temperature, alkalinity, and aragonite saturation state. Results showed that total alkalinity in a constant salinity decreased from the Larak Island located at the Strait of Hormuz to the Khargu Island in the northwest of the PG by 81 μmol/kg (S = 35) due to biotic and chemical calcification processes in the PG. AT-TCO2 plots allow us to further evaluate the effect of chemical and biological processes on the carbonate chemistry of seawater in the study area. The nAT-nTCO2 diagrams are shown in Fig. 6 for intertidal rocky 7

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Fig. 5. Daily variations of temperature, salinity, dissolved oxygen, pH, estimated aragonite saturation state and estimated pCO2 in seawater of the Hengam coral patch in September 2012 and January 2013.

reliable inorganic carbon source for calcification rather than the carbonate as the bicarbonate shows significantly smaller variability under natural environmental variations (Bach, 2015). However, the calcification rate of marine organisms often correlates well with [CO32−] and ΩCaCO3 due to the proportionality between these parameters and the ratio of [HCO3−] to [H+] (substrate to inhibitor ratio, SIR) at stable temperature, salinity and pressure (Bach, 2015). Among environmental variables, temperature shows significant positive effect on Ω and slight negative effect on SIR. When seawater temperature decreases the ratio

carbonate (CaCO3) with a profound impact on global biogeochemical cycles. Biotic calcification relies on calcium ions (Ca2+) and usually on bicarbonate ions (HCO3−) as CaCO3 substrates and can be inhibited by high proton (H+) concentrations. Studies show that in non-corrosive conditions (Ω > 1) net calcification rate is controlled positively by [HCO3−] and negatively by [H+] (Bach, 2015; Bach et al., 2011, 2015; Jokiel et al., 2014; Jokiel, 2011b; Jokiel, 2011a) rather than ΩCaCO3, where [HCO3−] serves as the inorganic carbon substrate and [H+] functions as a calcification inhibitor. The bicarbonate is a much more

Table 3 Seasonal variation in seawater carbonate parameters on the coral patch of Hengam Island compared to Davis reef in the central Great Barrier Reef (Albright et al., 2013). T = temperature, S = salinity, AT = total alkalinity, nAT = normalized total alkalinity to salinity of 35.0, TCO2 = total carbon dioxide, pCO2 = partial pressure of carbon dioxide, ΩAr = aragonite saturation. pCO2 (μatm)

ΩAr

7.92–8.17

275–542

2.9–4.1

8.15–8.23c

378–473

3.3–4.8

Location

T (°C)

S

AT (μmol/kg)

nAT (μmol/kg)

TCO2 (μmol/kg)

pHtotal

Davis reef (GBRa, 2012) (18.8°S) Hengam Island (PGb 2014–2015) (26.6°N)

22.1–28.9 (ΔT = 6.8)

34.9–35.7

2212–2322

2218–2277 (Δ = 59)

1878–2028

20.3–34.8 (ΔT = 14.5)

37.1–38.1

2411–2481

2275–2279 (Δ = 4)

2031–2122

a b c

Great Barrier Reef. Persian Gulf. pH in NBS scale. 8

scale

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ΩAr

ΩAr

SIR

Li near (ΩAr)

0.45

Linear (SIR)

8

0.4

7

0.35

6

0.3

5

0.25

4

0.2

3

0.15

2

0.1 20

b)

5.5 5

25

30

35

Temperature (°C)

40

ΩAr model for Hengam

ΩAr model for Kha rgu

ΩAr i n s amples of Hengam

SIR model for Hengam

SIR model in Khargu

SIR in samples of Hengam

0.5 0.45

4.5 0.4

4

ΩAr

3.5 0.35 3

2.5

0.3

2

0.25

[HCO 3-]/[H+] (mol/μmol)

9

a)

[HCO3-]/[H+] (mol/μmol)

Fig. 6. Total alkalinity versus total carbon dioxide diagrams by habitat type. Vectors illustrate the direction of the effects of photosynthesis and calcification on AT and TCO2. All data were normalized to a salinity of 35.

1.5

0.2

1 17

19

21

23

25

27

29

31

33

35

Temperature (°C) ̶ + Fig. 7. Aragonite saturation state (ΩAr) and substrate to inhibitor ratio ([HCO3]/[H ]) over different seawater temperatures. Graph a) shows the data of all locations and seasons (rock pools were excluded). Graph b) shows data for Hengam Island (solid lines) and theoretical trends for Hengam and Khargu Islands (dashed lines). To obtain theoretical trends using CO2SYS software, for Hengam Island, average input values for calculations were selected as: AT = 2445 μmol/kg, pCO2 = 430 μatm, S = 37.46 and temperature in the range of 22 to 35 °C and for the Khargu Island, average input values for calculations were selected as: AT = 2500 μmol/kg, pCO2 = 410 μatm, S = 39.6 and temperature in the range of 17 to 35 °C.

of [HCO3−] to [H+] increases slightly while, the saturation state of calcium carbonate declines significantly (Jiang et al., 2015; Jokiel, 2011a). This results in a large seasonal variation in [CO32−] and Ω (i.e. lower values in winter), and a very small seasonal variation in SIR. The influences of water temperature on the AT to TCO2 ratio, combined with

the temperature effects on the inorganic carbon equilibrium in seawater and the apparent solubility product of calcium carbonate (K'sp), explain these two different temperature effects (Jiang et al., 2015). Data of Ω and SIR in the intertidal rocky shores and coral reefs of the Persian Gulf and Makran sea (Table 2) against seawater temperature is shown in 9

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Fig. 7a and b. As it can be seen, both parameters show the same fluctuation patterns (mainly controlled by photosynthesis and respiration activities) with different trends (mainly controlled by temperature) in Hengam coral reefs in different months of the year (Fig. 7b) and all locations and seasons (Fig. 7a). Furtherly, to show the pure effect of temperature on Ω and SIR, assuming typical averages for AT, pCO2 and salinity in two coral sites and ignoring the variations in other environmental parameters (e.g. respiration and photosynthesis), SIR and Ω have been modelled for Hengam and Khargu Islands (Fig. 7b). Based on the model results, in coral patch of Hengam Island, increasing temperature from 22 °C in February to 33 °C in August could result in +39.3% and −6.2% changes in Ω and SIR, respectively. At the same period, seasonal warming from 17 °C to 33 °C in Khargu Island will result in +60.6% and −8.4% changes in Ω and SIR, respectively. Results obtained from field sampling-measuring in the coral habitat of Hengam Island also showed the same trends including fluctuations which have been induced by variable physical and biological conditions over the year (Fig. 7b). These seasonal trends show that inorganic carbon chemistry conditions for biotic production of calcium carbonate would be fairly constant over the wide range of intra-annual temperature variation in Hengam Island coral patch, if controlled by SIR, whereas, it would show a profound variation over a year, if determined by Ω. Although, the intra-annual variation of ΩAr in Hengam Island was obtained to be relatively large (37.5%), Vajed Samiei et al. (2016) found that the variation in the calcification rate of Acropora downingi is not significantly related to ΩAr (r2 = 0.02). Maybe, in the supersaturation condition of the Persian Gulf, the calcification rate of A. downingi is controlled by the [HCO3−] to [H+] ratio rather than the ΩAr. Also, data in Table 2 show that considering Ω as an indicator for calcifying environment in OLI, AFT and DBG near shores and rock pools suggest summer as the most favorable season, while SIR values in winter are more appropriate. Therefore, it can be concluded that in the Persian Gulf coral reefs and rocky intertidal shores which are supersaturated in term of calcium carbonate, due to the wide range of seasonal temperature variations, Ω is a poor indicator for evaluating the intra-annual suitability of the carbonate chemistry condition for calcification of some species. Although the SIR hypothesis requires further examination across a diversity of marine calcifying species, emerging evidence and mature conceptual theory on calcification are now available for corals, coccolithophores, and some bivalves, suggesting that SIR warrants the attention of the broader OA community (Fassbender et al., 2016). The lack of positive correlation between Ω and SIR especially in variable temperature and salinity has also been reported in both open ocean (Bach, 2015) and coastal areas (Fassbender et al., 2016). Fig. 8 shows the relation between [HCO3−] to [H+] ratio and ΩAr in the study area. Data of approximately similar seawater temperature (variation within 2.4 °C) were illustrated in two different categories (winter data, 22.2 to 24.6 °C, and summer data, 30.6 to 32.8 °C). Results show that in the study area, when temperature variations are limited to < 2.2 and 2.4 °C, correlation coefficients of 0.93 and 0.97 were obtained for SIR vs ΩAr in summer and winter, respectively. Therefore, due to the proportionality of Ω and SIR, both parameters could be considered as appropriate indicators for biotic precipitation of calcium carbonate when seawater temperature variations do not exceed ≈2.4 °C. Our data confirm that in order to better understand how OA will influence the ability of organisms to calcify in the shallow-water marine habitats with Ω > 1, it is important to consider the full carbonate chemistry and how it varies, rather than rely on a single carbonate system parameter.

Fig. 8. SIR-ΩAr diagram of data of approximately similar seawater temperature (variation within 2.4 °C). Blue circles show the wintertime data and red circles show the summertime data. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

chemistry in the easternmost and northernmost coral patches and rocky intertidal shores of the Persian Gulf together with two locations in Chabahar bay and Makran Sea coasts. The results reported herein address some of the gaps in the current understanding of carbonate chemistry and act as a starting point for further studies aiming to better understand these valuable habitats which are of major economic, ecologic, scientific, and social importance. It highlights the extreme variability in carbonate chemistry conditions experienced by shallowwater organisms of the region, an essential consideration for future ecological researches. To have a more precise perspective about the carbonate system in the study area measurements and samplings should be performed in a better temporal and special resolution including nighttime data. We are going to continue our monitoring projects in the region by improving the accuracy and precision of measurements (e.g. by direct measuring of pH in total hydrogen ion scale, dissolved inorganic carbon) to prepare for a part of the critical research needs for the future necessary protective measures in the Persian Gulf. Author contributions Abolfazl Saleh: conceptualization, methodology, investigation, validation, formal analysis, resources, visualization, Writing-Original draft preparation, project administration. Jahangir Vajed Samiei: conceptualization, investigation, formal analysis, Writing-Reviewing and Editing. Fatemeh Amini-Yekta: conceptualization, formal analysis, resources, visualization, Writing-Reviewing and Editing. Mehri Seyed Hashtroudi: methodology, investigation, resources, WritingReviewing and Editing. Chen-Tung Arthur Chen: conceptualization, validation, Writing-Reviewing and Editing. Neda Sheijooni Fumani: investigation, validation. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

4. Conclusions

Acknowledgments

Considering the lack of baseline carbonate system information in the Persian Gulf habitats, we reported the results of our recent studies on the spatial and, in some locations, temporal variability of carbonate

We would like to thank the Iran National Science Foundation (INSF) 10

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and the Iranian National Institute for Oceanography and Atmospheric Science (INIOAS) for funding this project in terms of sampling, field measurements and laboratory analysis. This work was conducted in the Project No. 93030701 founded by the INSF and as parts of projects No. 391-011-08 and No 393-SP-01-031 funded by the INIOAS. We also thank Dr. Kirsten Isensee (IOC-UNESCO), Dr. Katherine Schoo (IOCUNESCO), Jonathan Fin (SNAPO-CO2 laboratory), Dr. Behrooz Abtahi (INIOAS), Arash Shirvani and Ahmad Arabzadeh (INIOAS)for supporting this project.

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