Coral reef carbonate budgets and ecological drivers in the naturally high temperature and high alkalinity environment of the Red Sea

The coral structural framework is crucial for maintaining reef ecosystem function and services. In the central Red Sea, a naturally high alkalinity is beneficial to reef growth, but rising water temperatures impair the calcification capacity of reef-building organisms. However, it is currently unknown how beneficial and detrimental factors affect the balance between calcification and erosion, and thereby the overall growth of the reef framework. To provide insight into present-day carbonate budgets and reef growth dynamics in the central Red Sea, we measured in situ net-accretion and net-erosion rates (Gnet) by deployment of limestone blocks and estimated census-based carbonate budgets (Gbudget) in four reef sites along a cross-shelf gradient (25 km). We assessed abiotic variables (i.e., temperature, inorganic nutrients, and carbonate system variables) and biotic drivers (i.e., calcifier and bioeroder abundances). On average, total alkalinity AT (2346 - 2431 μmol kg−1), aragonite saturation state (4.5 - 5.2 Ωa), and pCO2 (283 -315 μatm) were close to estimates of pre-industrial global ocean surface waters. Despite these calcification-favorable carbonate system conditions, Gnet and Gbudget encompassed positive (offshore) and negative net-production (midshore-lagoon and exposed nearshore site) estimates. Notably, Gbudget maxima were lower compared to reef growth from pristine Indian Ocean sites. Yet, a comparison with historical data from the northern Red Sea suggests that overall reef growth in the Red Sea has likely remained similar since 1995. When assessing sites across the shelf gradient, AT correlated well with reef growth rates (ρ = 0.89), while temperature was a weaker, negative correlate (ρ = −0.71). Further, AT explained about 65 % of Gbudget in a best fitting distance-based linear model. Interestingly, parrotfish abundances added up to 82% of explained variation, further substantiating recent studies highlighting the importance of parrotfish to reef ecosystem function. Our study provides a baseline that will be particularly useful in assessing future trajectories of reef growth capacities in the Red Sea under continuous ocean warming and acidification.

Introduction degradation due to an increased intensity or frequency of extreme climate events (Eakin, 2001; residuals under a reduced model and type II partial sums of squares. Within each significant 206 factor, pair-wise post-hoc tests followed.

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A detailed account of benthic community structure in the study sites is outlined in Roik et al.

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(2015). In brief, a low percentage of live substrate (< 40 %) was characteristic of the sheltered 303 and lagoonal sites. In exposed sites (offshore and midshore) a community of calcifying 304 organisms took up to 48 % of benthos cover on average (hard corals and calcareous crusts).

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Major reef-building corals were the genera Acropora, Pocillopora, and Porites constituting 32-306 56 % of the total hard coral cover. biomasses of both parrotfishes and sea urchins were observed at the exposed nearshore site. midshore site, and then increased again towards the exposed offshore site. The inshore sites 318 along with the exposed midshore site exhibited the largest range of sea urchin size classes (from 319 categories 1 or 2 to the largest size class 5), while at the exposed sites, only the two smallest size 320 classes of sea urchins were recorded. The largest parrotfishes (category 5 parrotfish, i.e., > 45 cm 321 -69 cm fork length) were observed at the midshore sites and the sheltered offshore site. With the 322 exception of the exposed midshore site, category 1 (5 -14 cm) parrotfish were commonly 323 observed at all sites. In contrast, no category 6 parrotfish (≥ 70 cm fork length) were observed 324 during the surveys. based on the 30-months deployment of blocks ranged between -0.96 and 0.37 kg m -2 yr -1 (Table   331 2). G net for 12 and 30-months blocks were negative on the nearshore reef (between -0.96 and -0.2 332 kg m -2 yr -1 , i.e., net erosion is apparent), near-zero on the midshore reef (0.01 -0.06 kg m -2 yr -1 , 333 i.e., low net accretion), and positive on the offshore reef (up to 0.37 kg m -2 yr -1 , i.e., high net 334 accretion). Reef sites and deployment times had a significant effect on the variability of G net

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( Table S11). The rate of accretion/erosion was higher in the measurements over longest 336 deployment period (p < 0.001, Figure S2).  (Table 3). G budget significantly different between the reef sites (p < 0.05, Fig. 5 A), 343 except for budgets in both midshore sites (lagoon and exposed), which were similar. Biotic 344 variables that account for the carbonate budgets also differed by site, in the case of community 345 calcification rates G benthos (p < 0.05, Fig. 5 B), and net-accretion/erosion of bare substrate

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Results from correlations and distance based linear models were similar for G net and G budget .

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Temperature means, temperature SDs, and pH SDs were negatively correlated, while A T , Ω a , 352 CO 3 2-, and PO 4 3were positively correlated with G net (ρ ≥ |0.59|, Table 4). The best model for 353 G net data accounted for 56% (adjusted R 2 ) of the total variation. Here, A T alone explained 54% of 354 the data and was the only statistically valid predictor of two abiotic variables in the model (the 355 second being Ω a accounting for only 2% more, The difference between nearshore to offshore A T and Ω a in our study area was on average at a 421 range of 32 µmol A T kg -1 and 0.2 Ω a , respectively (Table S9) natural (e.g., species distribution, habitat preferences, reef rugosity) and/or anthropogenically-476 driven factors (e.g., differential fishing pressure; McClanahan, 1994;McClanahan et al., 1994). G budgets represent the cumulative contribution of the major biotic drivers of reef growth (G benthos , 508 G netbenthos , E echino and E parrot ) for each site (Glynn, 1997;Perry et al., 2012) and resulted in a net-509 erosive budget in the nearshore reef, low net-accretion (near zero) in the midshore reef, up to a 510 high net-accretion budget in offshore. Increasing across reef sites from nearshore to offshore, 511 G budgets imply that nearshore reefs currently erode with half the speed that the offshore reefs 512 grow, which may be interpreted as the formation of an offshore barrier reef in the central Red 513 Sea (see Figure 5). The cross-shelf dynamics of G budgets and the biotic drivers (G and E) are 514 complex and follow unique patterns that are in parts distinct from what we know from other reef 515 systems. Other than observed in the GBR, where reef growth is reported to be high at inshore 516 reefs (Browne et al., 2013), our nearshore study site, was net-erosive. Also, parrotfish erosion 517 was highest in the nearshore area in the present Red Sea study, whereas lower rates were 518 reported for the inshore reefs in the GBR (Hoey and Bellwood, 2007;Tribollet et al., 2002). On protected nearshore habitats), but these sites are typically characterized by a high coral cover 521 which drives a positive G budget (Perry et al., 2012(Perry et al., , 2014 . Unlike in the Red Sea nearshore reef, 522 which had the highest parrotfish erosion, but a negative G budget due to low coral cover. This inter-523 regional comparison demonstrates that patterns encountered in one cross-shelf reef system 524 should not necessarily be extrapolated to another system. In conclusion, in situ studies will be 525 required for each unique system to understand its dynamics and its responses to environmental 526 change.        between the reefs within each season (box: 1st and 3rd quartiles, whiskers: 1.5-fold inter-quartile 958 range, points: data beyond this range). A T = total alkalinity, Ω a = aragonite saturation state, C T = 959 total inorganic carbon; off = offshore, mid = midshore, near = nearshore, exp = exposed forereef, 960 shelt = sheltered lagoon, n.s. = not significant drying. Boring holes of endolithic sponges are clearly visible in the nearshore exposed and both 966 midshore reef sites. In the midshore and offshore exposed reefs, blocks were covered with crusts 967 of biogenic carbonate mostly accreted by coralline algae assemblages. EXP = exposed, SHELT = 968 sheltered, scales in E -H in cm. differences between the sites. Near_exp = nearshore exposed, mid_shelt = midshore sheltered 976 (lagoon), mid_exp = midshore exposed, off_exp = offshore exposed.