Intergeneric and geomorphological variations in Symbiodiniaceae densities of reef-building corals in an isolated atoll, central South China Sea

https://doi.org/10.1016/j.marpolbul.2020.111946Get rights and content

Highlights

  • Coral Symbiodiniaceae density (SD) shows intergeneric and spatial differences.

  • Corals with high SD in South China Sea (SCS) have stronger thermal tolerance.

  • Corals at outer reef slope of SCS atoll possess higher SDs than those at lagoon.

  • Corals in SCS Huangyan Atoll have higher SDs than those at neighboring reefs.

  • Human disturbances may limit the function of potential refuges for SCS corals.

Abstract

The healthy status of corals in the isolated atolls of the central South China Sea (SCS) remains unclear. Symbiodiniaceae density (SD) can effectively reflect the thermal tolerance and health of hard corals. Here, the SDs of 238 samples from the Huangyan Atoll (HA) were analyzed. The results revealed significantly intergeneric and geomorphological differences in SD. Intergeneric variation may reflect that corals with high SD have stronger thermal tolerance. Geomorphic analysis showed that the SDs at the outer reef slope were higher than in the lagoon. Hydrodynamics and sea surface temperature were likely the main influencing factors. Most notably, corals in SCS HA had higher SDs than those at neighboring reefs, indicating that their thermal tolerance were strong, which may be related to HA's local upwelling. These results suggest that the HA has the potential to serve as a refuge for corals, but increasing human disturbance limit its function.

Introduction

Coral reef ecosystems possess extremely high biodiversity and economic value (Bellwood et al., 2004; Costanza et al., 2014; Anthony, 2016). In their ecosystem, reef-building corals mainly rely on their relationship with the symbiotic dinoflagellates (i.e., Symbiodiniaceae) that provide them with essential nutrients for growth, calcification, and reproduction (Li et al., 2008; Oliver and Palumbi, 2011). Nevertheless, the increasing frequency and severity of abnormal sea surface temperatures (SST) and other local stresses could disrupt this symbiotic relationship. These can cause the Symbiodiniaceae to be expelled (Hoegh-Guldberg, 1999; Ban et al., 2014), which can eventually lead to coral bleaching and even mortality (Baker et al., 2004; Hughes et al., 2017; Hughes et al., 2018). Generally, this process also affects the growth and reproduction of reef-building corals, increases their susceptibility to various diseases, posing a serious threat to reef survival (Douglas, 2003; Hoegh-Guldberg et al., 2007; Baker et al., 2008; McClanahan et al., 2014). Furthermore, coral susceptibility to thermal bleaching is related to Symbiodiniaceae density (SD), and the higher the SDs, the stronger the resistance to bleaching (Baker et al., 2008; Li et al., 2008; Xu et al., 2017). Therefore, SD is considered to be a key indicator of corals' thermal tolerance and health (Jones, 1997; Wooldridge, 2014).

A growing number of studies highlight the influence of environmental factors on SD, including SST, salinity, solar radiation, nutrients, hydrodynamic regimes, and human activities (Smith et al., 2005; Wiedenmann et al., 2013; Ben-Zvi et al., 2019), leading to variations of SDs on interspecific, spatial and temporal scales (Xu et al., 2017; Qin et al., 2019a). In general, coral species that are more thermally tolerant or more adaptable exhibit higher SDs and are healthier (West and Salm, 2003; Berkelmans and van Oppen, 2006; Muir et al., 2015; Xu et al., 2017; Qin et al., 2019b). For example, in different species, SDs of branching Acropora species, which are the most vulnerable to bleaching, have been shown to be significantly lower than those of the massive corals (Marshall and Baird, 2000; Xu et al., 2017). Additionally, analyses of the SDs in different regions revealed that corals showed higher SDs in environments that could reduce the threat of thermal exposure (Qin et al., 2019a). Nevertheless, corals in shallower lagoons can also adapt to the fluctuating environmental conditions they endure on a daily basis and have become more resistant to bleaching stress, showing higher SDs (Grimsditch et al., 2010; Barshis et al., 2013). Variations in SDs therefore, reflect the corals' response to different environments (Wooldridge, 2014; Xu et al., 2017; Qin et al., 2019a, Qin et al., 2019b). Under the threat of global warming, it is necessary to identify more representative reefs worldwide by SD and, for each reef, describe the traits of present species, and the variation in local SST and current environmental conditions (Logan et al., 2014).

The South China Sea (SCS) with the highest coral diversity, borders the Coral Triangle, is an important part of the world's coral reefs (McManus et al., 2010; Yu, 2012). However, corals throughout the SCS have experienced several abnormal temperature events, leading to extensive coral bleaching and significant mortality, and its reefs are rapidly degrading (Hoegh-Guldberg, 1999; Hoegh-Guldberg et al., 2007; Zhao et al., 2012). Additionally, the El Niño events during 2015–2016, which was one of the most severe episodes since 1998, combined with the risks of overfishing, sedimentation, and marine-based pollution, seriously threatening the health of coral reefs in this area (Burke et al., 2011; Zhao et al., 2016; Tkachenko and Soong, 2017). Therefore, recent studies have focused on determining the SD in corals of nearly all of the coral reefs in the SCS, as these reflect, to some extent, the health status of coral reefs in the SCS (Li et al., 2008; Xu et al., 2017; Qin et al., 2019a). However, little attention has been paid to the coral reefs in the Huangyan Atoll (i.e., Scarborough Shoal), especially their Symbiodiniaceae of corals (Zhao et al., 2013, Zhao et al., 2016; Ke et al., 2016; Li et al., 2018). This serious knowledge gap is detrimental to the evaluation and protection of the entire coral reef ecosystems of the SCS (Harithsa et al., 2005; Berkelmans and van Oppen, 2006). Furthermore, studies have also found that despite the high susceptibility of reefs on remote atolls in the SCS to extensive bleaching and mortality due to various stressors, the potential for recovery of these isolated reefs is remarkable (Mora et al., 2016; Safaie et al., 2018; Chen et al., 2019b; Tkachenko et al., 2020). In short, the lack of research limits our ability to understand the ecological status of these reefs and predict their fate in a future subjected to increased warming and otherwise aspects of a changing climate. It may also overlook some reefs with potential functions.

The objective of this study is thus to analyze the SDs of corals collected in the Huangyan Atoll in May 2015, and to explore the effects of abnormally high temperatures on the coral reefs in this region, thereby, assessing the current ecological status and developmental trend of reef-building corals in the Huangyan Atoll under the climate change scenario.

Section snippets

Study sites

The Huangyan Atoll (HA; 117°40′–117°52′E, 15°05′–15°13′N), also named Scarborough Shoal or Democracy Reef, is located in the central SCS (Fig. 1). Its coral reef is roughly triangular, partially encircles a lagoon, and comprises an area of approximately 133 km2 with depths of 10–20 m. In the southeast, there is a passage (approximately 370 m wide and 3–11 m deep) connecting the lagoon and the open sea. Due to the micro–tidal regime (approximately 1.2 m), many coral reefs are submerged at high

Results

A total of 238 coral samples comprising 51 species of 11 genera within four families collected from the HA were analyzed in the present study (Tables 1 and S1). The SDs obtained for all species and geomorphologies ranged from 0.76 × 106 to 6.35 × 106 cells.cm−2, with an average of 3.12 ± 0.11 × 106 cells·cm−2 (n = 238), among which the Favia matthaii exhibited the highest average SDs while Acropora pulchra displayed the lowest. Overall, SDs varied greatly between corals in different genera and

Intergeneric variation of SDs and their relationships with coral tolerance to thermal stress

The results of the present study reveal that SDs vary greatly between coral genera in the HA, which is consistent with previous findings in the SCS (Li et al., 2008, Li et al., 2011; Xu et al., 2017). In general, the SD among coral genera is often linked to their thermal tolerance. Corals with strong tolerance to thermal stress tend to have high levels of SDs (Wooldridge, 2014; Xu et al., 2017). Therefore, we suggest that the SD variations in HA can also reflect the thermal tolerance of corals.

Conclusions

The analysis results of the SDs in corals showed that there were significant intergeneric and geomorphological differences in the HA. Specifically, SDs in massive corals were significantly higher than those in encrusting and branching corals, which may reflect a greater thermal tolerance of the former. In addition, Geomorphic analysis showed that the SDs of corals in the outer reef slope were higher than in the lagoon. Environmental conditions, such as hydrodynamic conditions and SST were

CRediT authorship contribution statement

This manuscript has not been submitted to other journals. All authors have seen the manuscript and agree to its submission to Marine Pollution Bulletin. The authors declare no competing financial interests.

Declaration of competing interest

The authors declare that there are no competing financial interests to the research.

Acknowledgements

This research was supported by the National Natural Science Foundation of China (Nos. 42090041, 42030502 and 41806139), the Guangxi Scientific Projects (Nos. AD17129063 and AA17204074), the Bagui Fellowship from Guangxi Province of China (2014BGXZGX03), and Science and Technology Planning Project of Guangzhou City, China (202002030345). The authors thank editor Paul Shin and two anonymous reviewers for their constructive comments which greatly helped the improvement of this manuscript.

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