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Physicochemical Dynamics, Microbial Community Patterns, and Reef Growth in Coral Reefs of the Central Red Sea

  • Anna RoikEmail author
  • Maren Ziegler
  • Christian R. Voolstra
Chapter
Part of the Springer Oceanography book series (SPRINGEROCEAN)

Abstract

Coral reefs in the Red Sea belong to the most diverse and productive reef ecosystems worldwide, although they are exposed to strong seasonal variability, high temperature, and high salinity. These factors are considered stressful for coral reef biota and challenge reef growth in other oceans, but coral reefs in the Red Sea thrive despite these challenges. In the central Red Sea high temperatures, high salinities, and low dissolved oxygen on the one hand reflect conditions that are predicted for ‘future oceans’ under global warming. On the other hand, alkalinity and other carbonate chemistry parameters are considered favourable for coral growth. In coral reefs of the central Red Sea, temperature and salinity follow a seasonal cycle, while chlorophyll and inorganic nutrients mostly vary spatially, and dissolved oxygen and pH fluctuate on the scale of hours to days. Within these strong environmental gradients micro- and macroscopic reef communities are dynamic and demonstrate plasticity and acclimatisation potential. Epilithic biofilm communities of bacteria and algae, crucial for the recruitment of reef-builders, undergo seasonal community shifts that are mainly driven by changes in temperature, salinity, and dissolved oxygen. These variables are predicted to change with the progression of global environmental change and suggest an immediate effect of climate change on the microbial community composition of biofilms. Corals are so-called holobionts and associate with a variety of microbial organisms that fulfill important functions in coral health and productivity. For instance, coral-associated bacterial communities are more specific and less diverse than those of marine biofilms, and in many coral species in the central Red Sea they are dominated by bacteria from the genus Endozoicomonas. Generally, coral microbiomes align with ecological differences between reef sites. They are similar at sites where these corals are abundant and successful. Coral microbiomes reveal a measurable footprint of anthropogenic influence at polluted sites. Coral-associated communities of endosymbiotic dinoflagellates in central Red Sea corals are dominated by Symbiodinium from clade C. Some corals harbour the same specific symbiont with a high physiological plasticity throughout their distribution range, while others maintain a more flexible association with varying symbionts of high physiological specificity over depths, seasons, or reef locations. The coral-Symbiodinium endosymbiosis drives calcification of the coral skeleton, which is a key process that provides maintenance and formation of the reef framework. Calcification rates and reef growth are not higher than in other coral reef regions, despite the beneficial carbonate chemistry in the central Red Sea. This may be related to the comparatively high temperatures, as indicated by reduced summer calcification and long-term slowing of growth rates that correlate with ocean warming trends. Indeed, thermal limits of abundant coral species in the central Red Sea may have been exceeded, as evidenced by repeated mass bleaching events during previous years. Recent comprehensive baseline data from central Red Sea reefs allow for insight into coral reef functioning and for quantification of the impacts of environmental change in the region.

Introduction

Coral reef ecosystems maintain a high species diversity, comparable to that of tropical rainforests, and they provide important ecosystem services such as provision of food, a source of income, and coastal protection (Reaka-Kudla 1997; Moberg and Folke 1999). The ecological and economic importance of coral reefs depends on the coral reef framework, which is essential for reef ecosystem functioning, as it provides habitats for reef species and thereby a foundation for ecosystem productivity (Graham 2014). Coral reefs are constructed by symbiotic reef-building corals that critically rely on sunlight and are limited to the warm and oligotrophic conditions of equatorial oceans (Buddemeier 1997; Wood 1999). These reefs predominantly exist in comparably stable physicochemical environments (Achituv and Dubinsky 1990; Wood 1999). Generally, reef-building corals live close to their upper thermal limit and are critically threatened by ocean warming (Wilkinson 1999). For this reason, coral reefs are among the ecosystems that are most susceptible to the consequences of global climate change (Hughes et al. 2003). Besides global stressors such as ocean warming and acidification, local stressors such as eutrophication, pollution, and overfishing also constitute a threat to coral reefs worldwide (Spalding and Brown 2015). Today, environmental limits of coral reefs, responses of reef biota to stressors, and their potential for acclimatisation, adaptation, and resilience under environmental change are arguably the most relevant topics in coral reef research (Kleypas et al. 1999; Gove et al. 2013; Palumbi et al. 2014; Mumby and van Woesik 2014; Ochsenkühn et al. 2017; Osman et al. 2017).

In this chapter, we present and characterise coral reefs in the central Red Sea and associated environmental conditions. Until recently access to this region was limited. Therefore, these reefs were sparsely studied and information about physicochemical conditions was commonly derived from remote sensing or short-term sampling events. However, in recent years the number of studies collecting in situ data from reefs in the central Red Sea has been growing (Berumen et al. 2013). We report on the most recent studies that provide comprehensive datasets and a baseline for coral reef research in this region. We begin by introducing the Red Sea coral reef ecosystems and describe the environmental regimes of coral reef habitats in the central Red Sea that demonstrate remarkable physicochemical structuring over spatial and temporal scales (Fig. 22.1). We discuss these environments in a global context and in relation to climate change. Next, we introduce biotic aspects of coral reefs, which are considered pivotal to reef functioning. We do this by presenting data on microbial (bacterial) communities that live in epilithic biofilms and that influence larvae recruitment of reef-building coral species. We also report on microbes that associate with reef-building corals and are assumed to contribute to coral health and fitness. After that, we address biological reef growth processes, the basis of reef habitat formation, including biogenic calcification and erosion (i.e., carbonate budgets). We highlight the measurable dynamics in the biotic realm and describe potential abiotic drivers of microbial community dynamics and reef growth processes in these coral reefs. We conclude by providing an overview of essential coral reef research questions to be addressed in this region.
Fig. 22.1

Central Red Sea coral reefs. The map shows the coastal region of the central Red Sea between Jeddah and Thuwal (near KAUST). Coral reefs in this area span environmental gradients, suitable for the study of coral reef functioning under various environmental conditions. The marked reef sites are located along two environmental gradients, a cross-shelf gradient (reefs 1–3, marked with squares; Roik et al. 2016) and an anthropogenic gradient (reefs 4–9, marked with circles; Ziegler et al. 2016) near the city of Jeddah (map prepared by Ute Langner, King Abdullah University of Science and Technology (KAUST))

Coral Reef Functioning in Challenging Environments—The Red Sea as a Case Study

The Red Sea is located in one of the warmest climate zones globally and is one of the most saline seas (Edwards and Head 1987; Sheppard et al. 1992). Due to its geographic location spanning latitudes that are considered high for coral reefs (up to 28°N), the Red Sea is exposed to seasonal changes of physicochemical conditions (Raitsos et al. 2013; Sawall et al. 2015; van Hoytema et al. 2016; Roik et al. 2016). It includes some of the warmest coral reef environments, yet harbours some of the most diverse reefs worldwide (Sebens 1994; DeVantier et al. 2000). The Red Sea features remarkable coral reef formations along its entire coastline (Edwards and Head 1987; Price et al. 1998), while the neighbouring region of the Persian/Arabian Gulf (PAG) hosts marginal coral reef communities that hardly support reef growth (Riegl 1999; Purkis and Riegl 2005).

In the Red Sea, challenging conditions such as high salinity and high temperature are paired with a remarkably high total alkalinity and aragonite saturation state, which are considered beneficial for calcification and reef growth (Kleypas et al. 1999; Allemand et al. 2011). In addition, little terrestrial run-off and high light penetration (Schlichter et al. 1986; Sultan et al. 2015) also favour coral reef accretion. Strong latitudinal gradients of temperature, salinity, and nutrients (Raitsos et al. 2013; Kürten et al. 2014) give rise to a variety of habitats which can in part be considered challenging for coral reefs, especially in the southern and central Red Sea, where average sea surface temperatures are highest. This unique combination of challenging and beneficial environmental conditions, as well as spatial gradients and seasonality make the Red Sea a valuable region to study coral reef dynamics. Reef-building corals and other reef organisms from these regions are expected to reveal physiological mechanisms and adaptations that can substantially contribute to the understanding of coral reef responses under environmental conditions that are predicted by global climate change projections. In this regard it is interesting to note that the northern Red Sea has been identified as a coral refuge, as it harbours corals that live well below their thermal threshold (Fine et al. 2013; Osman et al. 2017). Coral reefs of the Red Sea are increasingly threatened by environmental change and anthropogenic impacts alike (Atkinson et al. 2001; Loya et al. 2004; Raitsos et al. 2011; Ziegler et al. 2016), while their ecosystem functioning and global significance is not yet fully understood. In the following, knowledge from the coral reefs of the central Red Sea is discussed under the consideration of recently contributed insights into reef functioning in this still understudied region.

Physicochemical Conditions in Central Red Sea Coral Reefs: Challenging High Temperatures, Low Dissolved Oxygen, Beneficial Carbonate Chemistry

Environmental conditions in the central Red Sea partially deviate from conditions experienced in the majority of tropical coral reefs (Couce et al. 2012). Temperatures reach maxima of 33 °C (Davis et al. 2011; Roik et al. 2016) and the summer average exceeds the global mean temperature for coral reefs by 1.4 °C (Kleypas et al. 1999). At the same time, salinity is about 5 PSU higher than the global coral reef average of 34.3 PSU (Table 22.1). Slowing coral growth rates (Cantin et al. 2010), decreased summer calcification rates (Roik et al. 2015), and repeated coral bleaching events during recent years (Monroe et al. 2018; Furby et al. 2013) demonstrate that temperatures in the central Red Sea exceed the thermal limits of local reef-building corals. Together, challenging summer temperatures and high salinity levels in the reef habitats of the central Red Sea reflect future predictions of ocean warming (IPCC Working Group I 2013). Adding to this, dissolved oxygen on central Red Sea reefs occasionally decreases below concentrations of 2 mg L−1, which is commonly considered hypoxic and a stressor to marine life (Vaquer-Sunyer and Duarte 2008). Low dissolved oxygen levels reflect the trend of deoxygenation in marine habitats that is also predicted to take place with the progression of ocean warming (Keeling et al. 2010).
Table 22.1

In situ environmental regimes in coral reef habitats of the central Red Sea

Environmental variable

Central Red Sea

Worldwide(b)/GBR(c, d)

Temperature °C

24.0−33.0 [29.0]a

21.0−29.5 [27.6]b

Salinity PSU

38.4−39.8 [39.3]a

23.3−40.0 [34.3]b

Dissolved oxygen mg L−1

0.1−8.9 [3.5]a

2.1−10.8 [6.7/7.0]c

Nitrate and nitrite μmol L−1

0.1−1.0 [0.5]a

0−3.3 [0.3]b

Phosphate μmol L−1

0−0.10 [0.05]a

0−0.54 [0.13]b

Chlorophyll-a fluorescence μg L−1

0−3.4 [0.4]a

~0−4.0 [0.2/0.6]d

The table shows the annual minimum, maximum, and mean in brackets for the central Red Sea and for other coral reefs worldwide. GBR = Great Barrier Reef

References abased on continuous year-long measurements on reefs across the shelf, Roik et al. (2016); brange of estimated global averages for coral reefs [mean], Kleypas et al. (1999); crange of measurements on reefs at Heron Island (GBR) [means from two sites] [2]; drange derived from time series plots [lowest and highest mean from different reefs in the GBR], Schaffelke et al. (2012). Source Roik (2016)

With a dissolved oxygen concentration of about 2–4 mg L−1 in the central Red Sea, the dissolved oxygen level is 3–4 mg L−1 below what is measured at reefs, such as the Great Barrier Reef (GBR; Table 22.1), and also at reefs in the Gulf of Aqaba/Eilat (GoA) in the northern Red Sea (Badran 2001; Manasrah et al. 2006; Niggl et al. 2010). These low concentrations represent another aspect contributing to the challenging conditions for reef communities in the central Red Sea. Notably, these concentrations are likely driven by the comparatively higher temperatures that decrease oxygen solubility. While temperature data are routinely available from in situ measurements and remote sensing platforms, much less is known about the dynamics of dissolved oxygen in coral reef environments. In particular, only a few studies on coral reefs collected continuous dissolved oxygen data at a resolution that exceeded one sampling time per day. Hence, more continuous data and in-depth analyses of diel and seasonal patterns are needed to better understand the variability of dissolved oxygen on coral reefs and to estimate its effect on coral reef biota.

Despite some challenging conditions for coral reefs in the central Red Sea, other environmental factors are actually considered beneficial for benthic calcifying organisms and hence for reef growth. The Red Sea basin maintains a high total alkalinity (AT) and aragonite saturation state (Ωa) (Kleypas et al. 1999; Steiner et al. 2014), which support high biogenic calcification rates. A high buffering capacity of Red Sea waters against ocean acidification can be assumed. Therefore, coral reefs in the Red Sea grow under conditions that represent a sharp contrast compared to some marginal coral habitats, such as Bermuda, the eastern tropical Pacific including Galapagos and upwelling sites off Panama, where due to naturally low AT and Ωa, calcifying organisms are critically threatened by ocean acidification (Manzello et al. 2008; Yeakel et al. 2015) (Table 22.2).
Table 22.2

Carbonate chemistry of central Red Sea coral reefs and global comparison

Region (study)

AT (μmol kg−1)

Ωa

Central Red Sea (Roik et al. 2016)a

2.346–2.431

4.50–5.20

Global preindustrial values (Manzello et al. 2008)b

~2.315

~4.30

GBR (Uthicke et al. 2014)c

2.069–2.315

2.60–3.80

Puerto Rico, Caribbean (Gray et al. 2012)d

2.223–2.315

3.40–3.90

Bermuda (Yeakel et al. 2015)e

2.300–2.400

2.70–3.60

Panama, upwelling sites (Manzello et al. 2008)b

1.870

2.96

Galapagos (Manzello et al. 2008)b

2.299

2.49

alowest and highest means per reef site and season (aragonite saturation state Ωa calculations were based on total alkalinity and pH measured on the NBS scale); bestimated averages, for details see referenced study; clowest and highest means from reef sites during wet and dry seasons; dlowest and highest seasonal means from one site; eminimum and maximum from time series plots. Source Roik (2016)

Coral reefs thrive in the most oligotrophic parts of the oceans and low inorganic nutrient levels are essential to maintain healthy coral reefs (D’Angelo and Wiedenmann 2014; Rädecker et al. 2015). Hence, the highly oligotrophic conditions in the central and northern parts of the Red Sea (Silverman et al. 2007; Kürten et al. 2014) benefit coral reef health. Nutrient levels and chlorophyll-a in the central Red Sea are lower than in most other reef locations (Table 22.1), but concentrations increase to the south (Raitsos et al. 2013; Sawall et al. 2014). In particular, phosphate concentrations (~0.07 µM) were remarkably low in the central Red Sea compared to other coral reefs worldwide (~0.08–0.6 µM; Szmant 2002). During summer, phosphate levels are further depleted, while nitrate and nitrite levels remain almost unchanged (Roik 2016). Such a shift in the nitrogen:phosphorus (N:P) balance toward a higher ratio has been previously demonstrated to decrease the heat and light stress tolerance of symbiotic reef-building corals in aquarium experiments (Wiedenmann et al. 2013) and might prove particularly calamitous during the summer. Whether an increased N:P ratio also decreases coral stress tolerance in situ still requires verification. The naturally occurring inorganic nutrient ratios on the central Red Sea reefs offer an ideal case study to explore their influence on stress-resistance of coral communities in more detail.

Environmental conditions in central Red Sea reefs undergo spatio-temporal variability. This variability in many aspects is stronger than for many other tropical reefs. For instance, the annual temperature range spans up to 9 °C, which is 2–4 times larger than in most equatorial reefs (typically experiencing a range of 2–4 °C; Hume et al. 2013). This temperature range compares better to that of extreme regions that support marginal coral habitats, such as the Gulf of Oman (7 °C annual range) and the PAG (12–20 °C, Hume et al. 2013). While reef temperature and salinity fluctuate the most between seasons, dissolved oxygen and pH undergo strong diel fluctuations that reflect biotic feedback of respiration, photosynthesis, and calcification of coral reef biota (Bates et al. 2010; Drupp et al. 2011). Chlorophyll-a and sedimentation rates in the central Red Sea vary over the cross-shelf gradient (Roik et al. 2016). Reef habitats span a range from highly oligotrophic offshore sites to more productive nearshore waters (Fig. 22.1; Table 22.1). Given the dynamic physicochemical conditions in central Red Sea reefs, the region is ideal to study reef-building communities and individual reef organisms in response to seasonal change and their local acclimatisation to spatially separated and challenging environmental regimes.

The Role of Microbial Communities in Coral Reef Functioning

Coral reef research has historically focused on community composition of macrobenthic organisms such as corals and sponges (Benayahu and Loya 1977; Luckhurst and Luckhurst 1978; Done 1982), but more recently the role of microbial communities has come to the attention of research on coral reef functioning. Microbial communities are ubiquitous in coral reefs; they inhabit epilithic coral reef biofilms (Sawall et al. 2012; Witt et al. 2012), and they associate with key-organisms of the coral reef, such as corals and sponges (Rosenberg et al. 2007; Hentschel et al. 2012).

Microbial communities that live in marine biofilms play pivotal roles in coral reef functioning. These roles include contributions to nutrient cycles and ecosystem productivity (Wilson et al. 2003; Battin et al. 2003). Moreover, biofilms play a role in larval settlement and recruitment of reef-building corals (Heyward and Negri 1999; Webster et al. 2004). Bacterial communities vary depending on the presence of different algal exudates that select for specific and functionally differential bacterial taxa (Barott et al. 2011; Nelson et al. 2013; Haas et al. 2013). For instance, bacterial communities, which induce high settlement rates of coral larvae (Sneed et al. 2015), are typically sustained in epilithic assemblages in the presence of certain coralline algae species. In contrast, algal turfs and associated bacteria reduce the settlement of marine invertebrates and inhibit survival of coral recruits (Arnold et al. 2010; Barott and Rohwer 2012; Webster et al. 2015). As a result, coralline algae dominance is associated with sustainable coral recruitment and reef growth. Under unfavourable conditions (e.g., high nutrient levels or overfishing) this state can rapidly shift towards a community dominated by turf algae, which is then likely to further develop into (macro) algal-dominated states and lead to the degradation of the coral reef habitat (Littler and Littler 1984; Hughes et al. 2007).

Corals associate with unicellular dinoflagellate endosymbionts from the genus Symbiodinium and assemblages of other microorganisms (i.e., fungi, bacteria, archaea, and viruses), which together comprise the coral holobiont (Rohwer et al. 2002). These associations of microbial communities with reef-building corals underpin their success in oligotrophic, light-flooded warm oceans. Photosynthetic energy from Symbiodinium contributes substantially to the metabolic requirements and drives productivity of the coral host (Muscatine and Porter 1977). Carbon and nutrient cycling in the holobiont are further linked to the metabolism of the associated bacterial community (Rädecker et al. 2015). Bacterial associates are also suggested to play a crucial role in coral health and disease, and to fulfill symbiotic roles within the coral host (Rosenberg et al. 2007). Importantly, physiological acclimatisation to different habitats and environmental conditions can be achieved through changes of the associated microbial communities in the coral holobiont (Buddemeier and Fautin 1993; Reshef et al. 2006). Because microbial communities, both in biofilms and associated as symbionts in corals, have the potential to alter patterns and functioning of coral reefs, a better understanding of their environmental drivers and dynamics is of great relevance.

Insights from Community Dynamics of Epilithic Bacterial Biofilms

Among various bacterial habitats, such as the water column or in association with benthic invertebrates, epilithic biofilms stand out for their remarkable diversity of bacterial taxa (Table 22.3). Coral- and sponge-associated bacterial communities exhibit a lower diversity and typically display a highly structured composition often dominated by only a few bacterial families that reflect a selective bacterial habitat (Moitinho-Silva et al. 2014; Röthig et al. 2016b; Ziegler et al. 2016). In contrast, coral reef biofilms in the central Red Sea are characterised by a considerably higher diversity and richness (with up to 900 distinct Operational Taxonomic Units (OTUs) according to Chao1 estimator for species richness). A total of 16 bacterial families were dominant during the timeframe of a full year in all studied reef habitats from near- to offshore (Fig. 22.2a; Roik et al. 2016). Amongst these families were Rhodobacteraceae (Proteobacteria) and Flavobacteriaceae (Bacteroidetes) of which some taxa represent rapid surface colonisers and might act in the formation and maintenance of the biofilm (Dang et al. 2008). But, while some species of Rhodobacteraceae are also known to enhance coral recruitment (Sharp et al. 2015), others might act as pathogenic opportunists in coral disease (Sunagawa et al. 2010; Roder et al. 2014a, b). If biofilms were considered a reservoir of bacterial diversity that may provide a source of new taxa to the microbiomes of benthic invertebrates (e.g., reef-building corals), they may play an important role in contributing to organism disease or health, for example, through transmission of pathogens (Rosenberg et al. 2007) or provision of new physiological functions to the host (Bourne et al. 2016). Overall, implications and the potential of the high bacterial diversity and functions of certain bacterial taxa in coral reef biofilms are still unknown and warrant further study.
Table 22.3

Coral reef associated bacterial communities in the central Red Sea based on Operational Taxonomic Unit (OTU) richness and diversity

Bacterial habitat

Region of 16S rRNA gene

OTU richness estimate (Chao 1)

OTU diversity estimate (Inversed Simpson‘s Index)

Biofilm

16S V 3–4a

400–900d

6–160d

Seawater

16S V 3–4a

140–270d

4–13d

Seawater

16S V 5–6b

160–590e

2.5–7.8e

Coral

16S V 5–6b

80–300e

1.3–5.9e

Sponge

16S V 5–6c

300–700f

1.0–1.3f

OTU = operation taxonomic units, clustered at a similarity cut-off of 97%; aKlindworth et al. (2012); bAndersson et al. (2008); cSimister et al. (2012); dminimum and maximum per sample from Roik et al. (2016), eminimum and maximum per sample from Röthig et al. (2016b); Ziegler et al. (2016), only data from undisturbed sites are shown, coral species: Acropora hemprichii, Pocillopora verrucosa, Pleuractis (Fungia) granulosa;flowest and highest means from Moitinho-Silva et al. (2014), sponge species: Xestospongia testudinaria, Stylissacarteri. Source Roik (2016)

Fig. 22.2

Community composition and abiotic drivers of bacterial biofilms in the central Red Sea. Epilithic biofilm bacteria can influence macro-scale dynamics in the benthic community structure through their effects on the recruitment of invertebrate (in particular coral) larvae. Next-generation sequencing data of the bacterial 16S rRNA marker gene of year-long collected biofilm samples from the central Red Sea (a) reveal a dynamic community structure that is characterised by a remarkably high OTU diversity (Operational Taxonomic Units, 97% similarity). (b) In situ abiotic variables that were simultaneously assessed allow for the exploration of abiotic-biotic interactions. A non-Metric Multidimensional Scaling (nMDS) approach based on Bray-Curtis similarities and multivariate correlation analysis identifies temperature, salinity, dissolved oxygen (DO), and chlorophyll concentrations as potential abiotic drivers of community dynamics. (Source Roik et al. 2016, CC 4.0)

In the respective full-year study, bacterial community data were collected simultaneously with abiotic information across spatial and temporal scales allowing for the investigation of abiotic-biotic interactions (Roik et al. 2016), an approach that has been proposed recently for studying ecosystem functioning under consideration of natural variability and synergistic effects of multiple environmental drivers (Boyd and Hutchins 2012; Helmuth et al. 2014). Benthic bacterial assemblages in the central Red Sea reefs were dynamic along a cross-shelf gradient of reefs, but also between seasons. Their species (OTU) diversity increased during spring and summer when growth of epilithic algae on the reef surfaces was highest. This observation supports the notion of an interaction of algal and bacterial communities via the release of algal exudates that incite bacterial metabolism (Barott et al. 2011; Haas et al. 2013). Furthermore, the increase in algal cover and bacterial diversity coincides with the timing of coral reproduction in spring and early summer (Bouwmeester 2014) and deserves further specific investigation to understand the possible implications for coral recruitment in the central Red Sea.

Terrestrial run-off and chlorophyll-a were the most influential drivers/predictors of coral reef biofilm communities in the GBR (Witt et al. 2012). In comparison, in the central Red Sea a combination of multiple variables (i.e., temperature, salinity, dissolved oxygen, and chlorophyll-a; Fig. 22.2b) correlated best with community shifts, and hence, are likely to drive bacterial biofilm dynamics. Notably, these factors are predicted to change with the progression of global climate change (Keeling et al. 2010; IPCC Working Group I 2013). As a consequence, a restructuring of the bacterial assemblages is to be expected, and considering the role of biofilms in coral recruitment, benthic community structure is very likely to be affected from bottom-up (Heyward and Negri 1999; Marhaver et al. 2013; Jessen et al. 2014). The comparative evaluation of winter- and summer-specific community shifts can be considered a first step leading to a better understanding of the community dynamics that can be expected under ocean warming scenarios (Table 22.4). Bacterial OTUs that were significantly increased or decreased in the warmer seasons (Roik et al. 2016) can be considered candidates for temperature-sensitive taxa that presumably shift in abundance, responding to changes in temperature. Along these lines, this extensive data set on biofilms provides a basis and poses new research questions for future investigations.
Table 22.4

Candidates for temperature-sensitive bacterial taxa in epilithic coral reef biofilms in the central Red Sea

Increased abundances with lower temperatures (winter)

Bacterial species, family (Phylum)

Previously identified in

Reference (GenBank Accession#)

BLAST identity

Loktanella sp., Rhodobacteraceae (P)

Marine seabed sediments from an industrial harbor (Leghorn, Italy)

Chiellini et al. (unpublished) submitted (2012) (HE804021.1)

0.99

unclassified Phycisphaeraceae (PM)

Initial biofilm formation on electrochemical CaCO3 deposition (Red Sea, Eilat)

Siboni et al. submitted (2009) (FJ594871.1)

0.99

Fulvivirga sp., Flammeovirgaceae (B)

Coral reef biofilm (GBR, Australia)

Witt et al. (2011) (JF261960.1)

0.99

Fulvivirga sp., Flammeovirgaceae (B)

Coral reef biofilm (GBR, Australia)

Witt et al. (2012) (JQ727158.1)

0.99

Winogradskyella sp. (bootstrap 93%), Flavobacteriaceae (B)

Coral reef biofilm/crustose coralline algae (both: GBR, Australia)

Witt et al. (2011) (JF261857.1)/Webster et al. (2011) (HM177620.1)

0.99/0.98

unclassified Alphaproteobacteria (P)

Marine biofouling communities in heat exchanger

Taracido et al. (unpublished) submitted (2011) (GQ274234.1)

0.94

Increased abundances with higher temperatures (summer and fall)

Bacterial species, family (Phylum)

Previously identified in

Reference (GenBank Accession#)

BLAST identity

Gloeobacter sp., Gloeobacteraceae (C)

Initial biofilm formation on electrochemical CaCO3 deposition (Red Sea, Eilat)

Siboni et al. (unpublished) submitted (2009) (FJ594839.1)

0.99

unclassified Cohaesibacteraceae (P)

Scleractinian coral Acropora cervicornis (Caribbean)

Sunagawa et al. (2010) (GU118008.1)

0.99

Halomicronema sp., Pseudanabaenaceae (C)

Coral reef sediments (GBR, Australia)

Werner (unpublished) submitted (2006) (AM177412.1)

0.99

A4b (Ch)

Intertidal thrombolites (Bahamas, Caribbean)

Myshrall et al. (2010) (GQ484118.1)

0.99

unclassified Cystobacterineae (P)

Coral mucus (Red Sea)

Lampert et al. (2008) (EF576995.1)

0.97a

Rhodovulum sp, Rhodobacteraceae (P)

Microbial mat in hypersaline evaporation pond (Guerrero Negro, Mexico)

Kirk Harris et al. (2013) (JN446096.1)

0.98

unclassified Cystobacterineae (P)

Coral mucus (Red Sea)

Lampert et al. (2008) (EF576995.1)

0.97

unclassified Deltaproteobacteria (order: Myxococcales) (P)

Scleratinian coral Acropora palmata (Caribbean)

Pantos and Bythell (2006) (AY323192.1)

0.98b

Bacterial taxa with significantly differential abundance patterns between cold and warm seasons are listed, including information about previous occurrence of identical or highly similar bacteria. Best BLASTn hits with 100% sequence coverage are shown, except a= 95% and b= 97% sequence coverage. If not specified otherwise, species classification has a bootstrap value of 100%; P = Proteobacteria, B = Bacteroidetes, PM = Planctomycetes, C = Cyanobacteria, Ch = Chloroflexi; source Roik et al. (2016)

Insights from Community Dynamics of Coral-Associated Microbes

Reef-building coral species have distinct habitat preferences under which they perform at their best. They are also characterised by varying capabilities to acclimatise to changing environmental conditions. Their associated microbial symbionts represent a central component that influences acclimatisation and adaptation potential of the coral holobiont. Different Symbiodinium clades and species have different physiological and biochemical attributes, representing adaptations to distinct environments. These attributes can lead to differences in the performance of the coral host. For example, Symbiodinium clade D may confer increased thermal tolerance to its host, but leads to decreased growth rates in juvenile (Little et al. 2004) and adult corals (Pettay et al. 2015).

In the Red Sea, corals associate with a large diversity of symbionts from the genus Symbiodinium that encompass phylogenetic and physiological differentiated strategies. Typically, each coral specimen harbours one or two abundant Symbiodinium types and a few background types that occur at very low abundances (Ziegler et al. 2017a). In the Red Sea, the majority of endosymbiotic dinoflagellates in most coral species can be assigned to Symbiodinium clade C and to a lesser extend to clade D, while species-specific associations with clade A symbionts in corals from the family Pocilloporidae persist (Ziegler et al. 2017a). More specifically, clade C symbionts represent the largest diversity of all recorded Symbiodinium types in Red Sea corals and, interestingly, the prevalent but seemingly endemic type C41 was present in most coral hosts (Ziegler et al. 2017a). The ITS2 sequence of Symbiodinium C41 is highly similar to that of C1, and suggests a diversification event specific to the Red Sea that requires further investigation. In the similar environmental settings of the PAG, the prevalence of the locally adapted species Symbiodinium thermophilum confers a high thermal tolerance to its coral hosts (Hume et al. 2016). In the Red Sea, Symbiodinium C41 may represent a similar opportunity to explore adaptations of the coral symbiont to local conditions and its role in host adaptation.

The flexibility of the host-symbiont association plays a role in niche acclimatisation and ecological niche width of the coral holobiont. For example, two common coral species in the central Red Sea (Pocillopora verrucosa and Porites lutea) employ different strategies for niche acclimatisation in relation to the specificity of the coral-algae symbiosis. These coral species acclimatise between seasons and along environmental gradients of depth and distance to shore, either by establishing a specific symbiosis with a Symbiodinium type with a large physiological plasticity (P. verrucosa), or by forming different flexible associations with symbionts best adapted to the given environmental conditions (P. lutea; Ziegler et al. 2015a). The wide photoacclimatory potential of Symbiodinium can aid physiologically less flexible coral hosts like P. verrucosa to a relatively wide physiological niche as evidenced by the widespread occurrence throughout the Red Sea in this otherwise susceptible coral (Ziegler et al. 2014).

Host-symbiont associations may further limit and define light niches of corals as was first described for Pacific P. verrucosa and Pavona gigantea that harbour distinct Symbiodinium types and have distinct depth distributions (Iglesias-Prieto et al. 2004). In many coral species and locations the Symbiodinium community undergoes depth-dependent shifts and may thus increase the depth distribution of their coral host (Frade et al. 2008; Lesser et al. 2010; Cooper et al. 2011). In contrast, corals in the Red Sea from the genera Porites, Pachyseris, Podabacia, and Leptoseris each maintain stable Symbiodinium communities over a 60 m depth gradient (Ziegler et al. 2015b), similar to several species in the genus Agaricia in the Caribbean (Bongaerts et al. 2013). Data of the same Symbiodinium type associated with different coral hosts in the Red Sea further reveal an effect of the host on the physiology of the symbionts (Ziegler et al. 2015b), thus adding another level of complexity to how Symbiodinium community dynamics may contribute to niche acclimatisation in corals.

In contrast to coral-associated Symbiodinium communities that usually consist of only a few genotypes, coral-associated bacterial communities can consist of hundreds of taxa from many different phyla (Table 22.5). These diverse bacterial communities potentially entail a large diversity of functions that may benefit the host (Bourne et al. 2016). Thus, bacterial communities represent a significant potential for acclimatisation and adaptation of the coral holobiont (Bordenstein and Theis 2015; Ziegler et al. 2017b). Similar to the dynamics of the Symbiodinium community in the Red Sea, spatial and seasonal dynamics are also demonstrated for coral-associated bacterial assemblages. For instance, bacterial diversity in Ctenactis echinata from different central Red Sea reefs aligns with ecological differences between the sites, and bacterial composition is similar between reefs where these corals are abundant and successful (Roder et al. 2015). Microbial communities of Acropora hemprichii and Pocillopora verrucosa are structured according to the degree of anthropogenic impact and show a measurable anthropogenic footprint at polluted sites close to Jeddah, a city of over 4 million on the coast of the central Red Sea (Fig. 22.1; Ziegler et al. 2016). In these corals, host species-specificity of the microbiome is decreased at the most polluted sites (Ziegler et al. 2016). A similar pattern has also been observed in a mixed coral assemblage in the same area of impact, where microbial communities of hard and soft corals cluster by impact and not by host organism (Lee et al. 2012). This loss of species-specificity of the bacterial community has previously been reported in diseased corals across ocean scales (Roder et al. 2014b).
Table 22.5

Microbial taxon richness across corals from the central Red Sea based on metabarcoding of the ITS2 and 16S marker genes for Symbiodinium and bacteria, respectively

Coral genus

N

Symbiodinium OTUsa

N

Bacterial OTUs

Acropora

47

1–4

18

76–486b

17

104–908c

Ctenactis

  

42

14–145d

Pleuractis (Fungia)

7

2–4

32

62–865e

Pocillopora

35

1–4

18

69–201b

16

25–140f

Stylophora

23

2–6

32

58–527f

OTU = Operational Taxonomic Unit, determined at 97% similarity cut off

aall data from Ziegler et al. (2017a); bZiegler et al. (2016); cJessen et al. (2013); dRoder et al. (2015); eRöthig et al. (2016b); fNeave et al. (2016)

One of the best-known candidates for a bacterial coral-symbiont is found in the genus Endozoicomonas from the family Endozoicomonaceae (Neave et al. 2016). Endozoicomonas was one of the first bacterial associates to be localised in endodermal tissues of a scleractinian coral and was consequently proposed to be a significant member of the coral microbiome (Bayer et al. 2013; Neave et al. 2017). Bacteria from the genus Endozoicomonas are found in association with many coral species in the central Red Sea. These bacteria even dominate the microbiome with up to 75–90% in some specimens of Pocillopora verrucosa and Stylophora pistillata, respectively (Neave et al. 2017). Interestingly, each coral host species from the central Red Sea is associated with a distinct Endozoicomonas genotype, but specificity within different host species varies on a global scale (Roder et al. 2015; Ziegler et al. 2016; Neave et al. 2017). For instance, P. verrucosa harbours the same Endozoicomonas genotype throughout its global distribution range, while S. pistillata associates with geographically distinct genotypes (Neave et al. 2017). These different patterns were hypothesised to relate to the host species’ reproductive strategy, with higher geographic differentiation in brooding S. pistillata that transmits symbionts vertically and lower specificity in spawning P. verrucosa (Neave et al. 2017). However, the spawning coral A. hemprichii harbours distinct Enodozoicomonas genotypes between the polluted reef area close to Jeddah (Ziegler et al. 2016) and the more pristine area off Thuwal, 100 km to the north (Jessen et al. 2013). This indicates that other factors, for example, environmental stressors such as pollutants may also play a role in host-bacterial symbiont specificity. Indeed, the relative abundance of Endozoicomonas in coral microbiomes could be linked to habitat suitability, as illustrated in decreasing abundance toward less preferred/optimal habitats (Roder et al. 2015; Ziegler et al. 2016).

To date, the significance and functions of bacterial associates of the coral holobiont are largely unknown, although their role in coral health and disease has long been discussed (Rohwer et al. 2002; Reshef et al. 2006; Rosenberg et al. 2007; Bordenstein and Theis 2015). Analyses of whole genome sequences of several Endozoicomonas species, including taxa from Red Sea corals, indicate roles in sugar transport and protein secretion that may contribute to carbon cycling within the coral holobiont (Neave et al. 2014). Furthermore, in situ data suggest that restructuring of the microbiome could mediate environmental tolerance of the coral Pleuractis (Fungia) granulosato increased salinity (Röthig et al. 2016b). The bacterium Pseudomonas veronii was identified as one of the main contributors to putative functional shifts in the microbiome under high salinities. The same bacterial taxon was further found to be highly abundant in mucus from Porites spp. colonies in the Red Sea and PAG (Hadaidi et al. 2017), both regions characterised by high salinity, and thus it represents a second symbiotic candidate taxon in Red Sea corals. It is not yet clear to what degree bacterial communities influence holobiont physiological performance (Bourne et al. 2016), or interact with the Symbiodinium-coral symbiosis (Röthig et al. 2016a). Only recently, Pogoreutz et al. (2017a) identified a potential link between bacteria and coral bleaching and also showed that susceptibility of bleaching is associated with diazotroph (i.e., nitrogen-fixing bacteria) abundance (Pogoreutz et al. 2017b). Although progress has been made in deciphering functional aspects of coral-associated microbial community dynamics, future research employing functional microbial ecology approaches to the coral holobiont framework are necessary to further improve our understanding.

Biological Reef Growth Processes: Calcification and Carbonate Accretion as a Measure of Coral Reef Persistence

The coral reef framework provides a living space for a range of highly diverse and productive coral reef biota (Graham 2014; Rogers et al. 2014). Not only calcification, but also processes of carbonate removal, i.e., erosion and dissolution, simultaneously influence the formation and maintenance of the reef framework (Glynn 1997; Perry and Hepburn 2008). Calcification of benthic communities (corals and coralline algae) contributes to reef growth, while dissolution and bioerosion by parrotfish, sea urchins, and endolithic bioeroders decrease reef growth and can lead to degradation of reefs when erosion rates exceed accretion (Glynn and Manzello 2015). A positive carbonate budget ensures the persistence of reef habitats, and is the result of high abundances of reef-builders and high calcification rates, which surpass rates of erosion. The estimation of carbonate budgets (i.e., carbonate net-production states) has proven valuable in identifying the state of reef ecosystems and quantifying potential reef degradation (Alvarez-Filip et al. 2009; Perry et al. 2013; Kennedy et al. 2013). Many coral reefs worldwide are characterised by negative (net-erosive) carbonate budgets, that are often related to an increased frequency of extreme climatic events (Eakin 2001; Schuhmacher et al. 2005) or local human impacts, such as pollution and eutrophication (Edinger et al. 2000; Chazottes et al. 2002).

Environmental factors that influence calcification and erosion processes drive carbonate budgets. Temperature and carbonate chemistry are the most influential factors for calcification, implying the susceptibility of calcifying organisms to ocean warming and acidification (Clausen and Roth 1975; Schneider and Erez 2006; Anthony et al. 2008; McCoy and Kamenos 2015). On the other hand, erosion is usually higher in turbid and nutrient rich habitats, because these are the preferred habitats of endolithic bioeroders (e.g., boring sponges, clams, and worms) (Pari et al. 1998; Chazottes et al. 2002). Also, low pH and a reduced carbonate saturation state can increase erosion rates (Wisshak et al. 2012; Fang et al. 2013) while reducing the calcification capacity of reef-builders, that leads to an additive negative effect of ocean acidification on overall reef growth.

Insights from Coral Reef Calcification in the Central Red Sea

Calcification is a temperature sensitive process. Observations along latitudinal temperature gradients have demonstrated that increasing temperatures, which remain below a certain threshold, enhance calcification rates in reef-building corals (Lough and Barnes 2000; Carricart-Ganivet 2004). However, when a critical thermal limit is exceeded, calcification rates decline as a result of thermal stress (Marshall and Clode 2004). Consequently, ocean warming compromises calcifying organisms. Specifically in reef-building corals, thermal stress disturbs the coral-dinoflagellate symbiosis and thereby is interfering with an important energy supply needed to maintain high calcification rates (Weis 2008). The study of reef calcification in the Red Sea is of interest, on the one hand, because it is one of the warmest regions with significant coral reef formations and has been affected by comparably high warming rates over the past decades (Belkin 2009), both aspects being considered challenging for calcifying marine organisms. On the other hand, the carbonate chemistry in the Red Sea is comparable to coral reef preindustrial estimates and is considered beneficial for biogenic calcification (Gattuso et al. 1999).

Pelagic carbonate precipitation rates in the Red Sea were estimated to be higher than in the Gulf of Aden or the Indian Ocean (Steiner et al. 2014). In spite of this, benthic calcification rates of corals and coralline algae from the central Red Sea were not higher than elsewhere. For instance, the annual average calcification rates for the major reef-building coral genera Porites, Acropora, and Pocillopora did not exceed rates measured in other parts of the world (Roik et al. 2015).

Calcification in the reefs of the central Red Sea might be on a trajectory of decline. First, calcification rates of Diploastrea heliopora, a massive-growing reef-building coral species, have decreased in correlation with gradually increasing sea surface temperatures over the past few decades (Cantin et al. 2010). Furthermore, Porites, Acropora, and Pocillopora exhibit an unusual seasonal pattern of calcification maxima during the cooler seasons rather than during summer, which is when calcification maxima are observed in a majority of other coral reefs worldwide (Crossland 1984; Hibino and van Woesik 2000; Kuffner et al. 2013). One possible explanation is that high temperatures during summer exceed the optima for calcifying organisms and limit their capacity for calcification. Also, coral bleaching events in the central Red Sea during the last decade support the notion that the thermal limits of many coral species have already been reached and exceeded (Monroe et al. 2018; Furby et al. 2013). However, it remains unresolved whether other conditions that are characteristic for the summer, for example, reduced dissolved oxygen and phosphate depletion, may contribute to the decrease in calcification of corals during the warmest season.

High summer temperatures challenge calcifying organisms in the central and southern Red Sea, but not in the northern region where growth rates in various coral species (Stylophora pistillata, Pocillopora damicornis, and Acropora granulosa) reach their peaks in summer (Kotb 2001; Mass et al. 2007). In line with this, calcification in the coral P. verrucosa has an inverse seasonal pattern along the latitudinal gradient of the Red Sea basin. Calcification maxima occur during summer in the northern Red Sea, and during winter in the south, indicating limited adaptation to local environmental conditions in the central and southern parts (Sawall et al. 2015). It remains unclear whether other important reef-building corals follow the same latitudinal pattern, unless further in situ data from the southern region will be acquired to complement the findings from the central Red Sea (Roik et al. 2015).

Carbonate Budgets in the Central Red Sea

Estimates of carbonate budgets, or reef net-production states, mainly rely on in situ measurements of calcification and erosion rates in combination with census-based data to approximate the cumulative contribution of all biotic drivers of reef growth. These encompass benthic calcification rates and erosion rates of endolithic organisms and surface grazers, such as sea urchins and most importantly parrotfish (Glynn 1997; Perry et al. 2012).

Very few carbonate budget data are available from the Red Sea (Jones et al. 2015). The first comprehensive account of reef growth in the Red Sea is from the Gulf of Aqaba in the northern Red Sea and shows calcification rates of corals, bioerosion measurements, and fossil reef growth estimates on a fringing reef (Fig. 22.3a and c; Heiss 1995; Dullo et al. 1996). Recently, carbonate budgets have been studied on central Red Sea reefs demonstrating a wide range of carbonate net-production states (Roik 2016). Reefs are characterised by net-erosion states in nearshore areas, while midshore and offshore reefs are in net-accretion states (Fig. 22.3a). According to these estimates, offshore reefs currently grow at twice the rate that nearshore reefs erode. The overall reef net-production states from the Red Sea are within the range of carbonate budgets from a variety of coral reefs worldwide (Fig. 22.3a and b; Eakin 1996; Edinger et al. 2000; Perry et al. 2013), but distinctly below the highest recorded budgets from remote and mostly unimpacted tropical reefs in the Indian Ocean (Fig. 22.3; Chagos Archipelago; Perry et al. 2015).
Fig. 22.3

Ranges of modern-day and preindustrial coral reef carbonate budgets. Carbonate budgets are a promising tool to track the trajectories of historical, modern-day, and future reef growth. (a) Central Red Sea reef budgets exceed the highest budgets of a northern Red Sea fringing reef (Dullo et al. 1996) and of the marginal reefs in (b) the Eastern Pacific (Eakin 1996). Yet, these budgets are below the maxima from several other (often remote and minor impacted) coral reefs worldwide (Indonesia, Edinger et al. 2000; Caribbean, Perry et al. 2013; and Chagos Archipelago, Perry et al. 2015). (c) Preindustrial estimates are based on fossil reef core analysis or a modelling approach (Hubbard et al. 1990; Dullo et al. 1996; Enochs 2015). In particular within the Red Sea, comparisons of modern-day carbonate budgets with historical estimates remain elusive due to sparseness of data. GoA = Gulf of Aqaba; preind. = preindustrial; only means of preindustrial reef growth are reported from the Red Sea (GoA) (Dullo et al. 1996)

In the central Red Sea, biotic and abiotic variables shape reef growth. Carbonate budgets aligned with the abundance of parrotfish and also with the abundance of calcifying organisms (Roik 2016). Interestingly, total alkalinity was positively correlated with reef growth in the central Red Sea along the cross-shelf gradient, but differences along this gradient were in a relatively small range (~20–50 μmol kg−1) (Roik 2016). Multiple laboratory, mesocosm, and in situ studies in various coral reefs report the positive relationship of benthic calcification and abiotic carbonate system variables, such as total alkalinity or carbonate saturation state (Langdon et al. 2000; Schneider and Erez 2006; Bates et al. 2010). The decrease of these variables due to ocean acidification in many reefs worldwide may compromise carbonate production in the future (Gattuso et al. 1999), but the beneficial carbonate chemistry in the Red Sea may delay the arrival of critically low total alkalinity and carbonate saturation due to ocean acidification in this region. Yet, the notable influence of total alkalinity on reef growth in the central Red Sea indicates that even minor shifts in carbonate chemistry may bear large consequences for reef growth.

As has been discussed previously, ocean warming is one of the major threats to calcifying organisms in the central Red Sea. As calcification rates have slowed over the past decades and are generally decreased during the warm season (Cantin et al. 2010; Sawall et al. 2015; Roik et al. 2015), it is important to elucidate whether overall reef growth in the central Red Sea is already impaired compared to historical rates of reef growth. Here, we compare recent carbonate budget estimates from the Red Sea with estimates of fossil reef growth rates during the Holocene (Fig. 22.3c; Hubbard et al. 1990; Enochs 2015). The lack of historical data from the central Red Sea impedes a direct comparison of the present-day budgets (Roik 2016) with reef growth in the past. The remaining comparison with 1995 estimates from the northern Red Sea (Dullo et al. 1996) leads to the notion that reef growth in the Red Sea has not decreased over the past decades (Fig. 22.3c). However, the latitudinal gradient of temperature, salinity and nutrients between the northern and the central Red Sea likely hampers this direct comparison. In order to consolidate this assumption further study of historical and present-day reef growth is required.

Carbonate budgets are a promising tool to track the trajectories of modern-day and future reef states (Perry et al. 2012; Enochs 2015). Such data will be particularly valuable when evaluating the impact of disturbances in central Red Sea reefs. For this, the most recent carbonate budget study from 2014 (Roik 2016) may also prove a useful reference point to evaluate the impacts of the third global bleaching event 2015/2016 on coral reefs in the Red Sea (Monroe et al. 2018).

Conclusions and Outlook

The central Red Sea is as a highly interesting region for coral reef research because of its spatially and seasonally dynamic environment, challenging conditions, and highly productive reef ecosystems. The recent accumulation of in situ environmental data and insights from the microbial ecology of reef biofilms and corals provide new avenues for research questions to be addressed for coral reefs of this region (Box 1).

Seasonal variability, high temperatures, high salinity, and low dissolved oxygen make the central Red Sea a challenging environment for coral reef biota whose mechanisms of acclimatisation and adaptation to these conditions are yet to be understood. The specific environmental conditions in the Red Sea allow for the in situ study of the influence of shifting inorganic nutrient (N:P) ratios on coral stress resistance. This may lead to a better understanding of the nutrient equilibrium between the different compartments in the coral holobiont and their relation to thermal stress susceptibility.

Coral reef biofilms in the central Red Sea harbour bacterial communities, which undergo seasonal cycles linked to the environmental dynamics. Comparison between winter and summer bacterial communities of biofilms have guided the identification of temperature-sensitive taxa, whose effect on coral reef functioning is likely to change with projected warming trends under global climate change. Biofilm communities are of remarkably high bacterial richness and diversity. Beyond their influence on processes such as recruitment of reef biota, the relation between diverse bacterial biofilm communities and the microbiomes of benthic reef invertebrates is unexplored and warrants further investigation. For instance, the consequences of a putative transmission of bacterial taxa from biofilms to corals and possible effects to coral host fitness remain to be determined. Understanding the dynamics, interactions and functions of these microbial taxa will enable us to better predict the consequences of, for example, temperature-related shifts on the coral reef ecosystem.

Future research should also aim toward understanding the functional aspects of coral-associated algal community dynamics in the central Red Sea. For instance, the locally prevalent Symbiodinium type C41 represents an opportunity to explore adaptations to local conditions in the Red Sea as previously described for S. thermophilum in the Persian/Arabian Gulf (PAG). Furthermore, although much progress has been made in understanding the role of the bacterial coral-associate Endozoicomonas, experimental investigation should focus on elucidating its putative functions in the coral holobiont. In this regard, targeted functional profiling of other candidate taxa, such as P. veronii, may also increase our understanding of coral holobiont functioning. Lastly, understanding the influence of stressors on species-specific associations between corals and bacteria, such as the decrease of Endozoicomonas under adverse environmental conditions, will be critical in determining and better understanding coral health states.

Repeated bleaching events and decreases in coral growth rates testify to the direct impact of global warming on coral reefs in the central Red Sea. In addition to high temperatures, other factors such as high salinity and low dissolved oxygen concentrations may be aggravated with the progression of climate change in the region, and the cumulative effects of these changes on coral growth and stress susceptibility remain elusive. The baseline of abiotic and reef growth data allows for tracking of the effects of disturbances, such as coral bleaching events, on overall ecosystem health. In the face of the global coral bleaching event of 2015/2016, these data are valuable for assessing long-term impacts and to track the recovery processes, which will provide insight into the resilience of central Red Sea coral reefs.

Box 1. Knowledge gaps in coral reef functioning of central Red Sea reefs

  • detailed understanding of acclimatisation and adaptation mechanisms in reef biota to variable and challenging environmental conditions

  • influence of shifting inorganic nutrient (N:P) ratios on coral stress resistance

  • role of temperature-sensitive bacterial taxa in coral reef biofilms

  • potential transmission of bacterial taxa from biofilms to corals and consequences for host fitness

  • locally adapted Symbiodinium types (e.g., type C41)

  • role of Endozoicomonas in the coral holobiont

  • osmoregulation of the different compartments of the coral holobiont

  • relationship between loss of bacterial species-specificity and reduced host-fitness

  • cumulative effects of warm summer temperatures and other stressors on coral calcification and stress resilience

  • comparison of recent and historical carbonate budgets, assessment of the impact of the third global bleaching event of 2015/2016 on coral reef growth

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Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Anna Roik
    • 1
    • 2
    Email author
  • Maren Ziegler
    • 2
    • 3
  • Christian R. Voolstra
    • 2
  1. 1.Marine MicrobiologyGEOMAR Helmholtz Centre for Ocean ResearchKielGermany
  2. 2.Red Sea Research Center, Division of Biological and Environmental Science and Engineering (BESE)King Abdullah University of Science and Technology (KAUST)ThuwalSaudi Arabia
  3. 3.Department of Animal Ecology and SystematicsJustus Liebig University GiessenGiessenGermany

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