Chapter – II: (implemented March 2005) - Main Page

Rather than being unitary organisms that follow a predetermined body plan, corals are modular organisms. Contrary to the predictable succession of developmental phases of individual organisms, modular organisms can proliferate on one end while at the other polyps may be already in the phase of decomposition. Indeed, death in such organisms often results from becoming too big or succumbing to disease rather than from programmed senescence (fig.2.2). Thus, the body of an individual modular organism has an age structure – it is composed of young and developing, actively functioning and senescent parts.

Based on environmental factors this modular concept enable corals to perform vertical, horizontal growth or a combination of both (see chapter-I, figure 1.9). With no mobility (except mobile forms such as Fungiidae), coral architecture determines interaction with its environment. Like in trees, most of the structure of stony corals is dead, with a thin layer of living material covering the exoskeleton. The individual polyp may exist as a physiologically integrated whole (e.g. Fungiidae), or may be split to shape a colony that forms one whole individual, but physiologically independent (e.g. Acroporidae).

Figure 2.3 highlights the morphological features of a coral colony and the main secreting agent responsible for the massive bioherm structures – the thin living veneer that covers reef-building corals. Since the morphological features drastically vary among species, skeletal shape and structure are the most obvious manifestation and the most accessible feature for identification and classification of hermatypic corals.^2.4 The key element in the cnidarian body plan is the polyp. It is a hollow cylindrical blind-ended sac forming a mouth, which is surrounded by a ring of hollow retractable tentacles. Compared to the often massive structure of the colony, the polyps are usually small fleshy extensions of the coral cover. Epithelio-muscular cells (myonemes) and the subepidermal nerve net provide the polyps with the ability to expand or contract their tentacles, detect changes in the environment, and communicate with other polyps in the colony. The pharynx constitutes the bottleneck between the tentacles the partitioned gastric cavity (although both tentacles and mesenteries - as the entire animal - form one continuum, they have been named separately for practical reasons).

The free edges of the mesentieries form mesenterial filaments (some corals extrude them to “digest” the living tissues of neighboring competitor species - see fig.5.15a, Chapter V). The living tissue is simply composed of two cell layers, the epidermis (also called ectodermis) and the gastrodermis (sometimes referred to as endodermis). Polyps of colonial corals are linked by a common gastrovascular tube-system, which take over the function of circulation and digestion. The epi- and gastrodermal layers are separated by a thin layer of gelatinous connective tissue, the mesogloea and are composed of collagen fibers, muco-polysaccharides, and cells. Although generally referred to as mesogleal cells, they represent different cell populations, in that some appear to be fibroblasts (secreting the matrix and collagen fibers) while others, called amoebocytes, can be granular or agranular (and are capable of phagocytosis).

In fact, some of these cells have been identified as pluripotential stem cells, capable of dividing and differentiating into various cell types as needed, such as cnidoblasts, scleroblasts, or germ cells.^2.6 The lower epidermal layer (calcioblastic epithelium) of the polyps secretes the aragonite exoskeleton. The interface between the polyp sac and the exoskeleton is lined by desmocytes, which attach the polyps to their supporting Calcium-Carbonate exoskeleton. The external epidermis covering the surface of the polyp, including the interpolypal tissue or coenosarc (coenenchyme) is made of a simple columnar epidermis (pseudostratified columnar epithelium). A cuboidal epithelium covers the layer of mesogloea, the gastric cavity and the gastrovascular canals (the mesenteries and their filaments within the gastric cavity are lined on both surfaces by gastrodermis with only the mesogloea in-between). The various cell types within the external and internal epithelial layers not only provide protection and enable the polyps to capture and digest food, but they also support endosymbiotic dinoflagellates in their relationship with its host coral (see fig.2.4a).
Unicellular secretory (gland) cells and ciliated supporting cells are embedded in the upper epidermis (the same is true for the gastrodermis). These gland cells build up a stratum that constitutes the interface between the external surface and the seawater. It has been termed the Muco-Poly-Saccharide Layer (MPSL), is made up of lipids, hydrophilic polysaccharids, proteins and produces a lubricating, mucilaginous surface layer. MPS can associate with proteins to form mucoproteins, which have much longer polysaccharide components than glycoproteins, are amorphous, and form gels able to hold large amounts of water.^2.7 This mucus-rich surface microlayer is highly productive. Their thickness can vary from less than 1mm in some scleractinians, to a few centimetres in some gorgonians.^2.8 Thus, their chemical composition (both qualitatively and quantitatively) does result in different microbial associations among species.^2.9 In fact studies have shown that corals of the same species have similar microbial communities even when separated by hundreds of kilometres, while microbiotas associated with different coral species are distinct even when the colonies are immediately adjacent to one another.^2.10 They do so by secreting fixed carbon in the form of specialized mucus.^2.11 The fact that among different species there is no universal chemical composition to coral mucus is further underlined by the difference in the ratio of protein to carbohydrate, glucose content, and amino acid composition suggests that these differences are species-specific and used in allo-recognition.^2.12 On the other hand diurnal fluctuation should not deter the beneficial microbial community to abandon the mucosal substrate, as both physical and chemical changes within the MPSL can oscillate in dynamic fashion. During the day when the endosymbionts carry out photosynthesis, the mucus layer is supersaturated with oxygen. Quite the opposite occurs under aphotic conditions. Here coral respiration depletes the oxygen levels to almost anaerobic levels.

Disrupting this relationship between microbes and corals has the potential to cause havoc and therefore cause collapse to the whole community.^2.13 Under favorable growth conditions, such pathogenic strains become opportunistic especially where this membrane is poorly developed (stressed coral animal) or even bleached. Indeed, the epidermis at the base or sediment margin of massive corals lacks mucous secretory cells, making it easier for diseases such as WPL and BBD to manifest themselves as they typically originate at these tissue margins.^2.14 Bacteria in contact with host tissue at the mucous membrane may be associated either loosely or firmly. The former are easily swept away, while the latter attach to the epithelial surface (as a result of specific cell-cell recognition between the microorganism and the host). From there actual tissue infection may follow.^2.15a

Even though, the physical structure of MPSL and their associated microbial communities have not been studied in detail, there are strong indicators that environmental changes affect the physiological equilibrium between bacteria already present in the normal flora associated with coral reef organisms (i.e. tissues and mucus) and their hosts, or stimulate other bacteria living in reef sediments into becoming virulent and thereby contributing in coral-related diseases.^2.16

Coral Physiology: Even though the energetic pools on a reef seem so large (i.e. photosynthetic active radiation, PAR, dissolved nutrients, organic material, etc.) one should not forget that they are spread (diluted) over huge areas. And still the relatively small differences in net energy fluxes (between inputs and outputs) are still large in absolute terms. If just one of these intrinsically inter-connected fluxes is disturbed (export of secondary trophic consumers – usually in the form of overfishing), then the determinants and the magnitude of the overall flux will be altered, resulting in disturbing feedback loops that changes the bias of reef survival from a slight benefit to a net disadvantage.^2.17 Indeed, the resulting alterations of both production and decomposition processes on coral reefs are not just restricted to the community level, but go all the way down to the structural level of the coral animal - to the physiological, physiographic level (this feature is not just restricted to reef ecosystems, but is found throughout the biosphere and emphasizes the holistic principles of community stability).

Heterotrophic Nutrition: As indicated in Chapter-I (trophic complexity), hermatypic corals are neither entirely heterotrophs, nor rely solely on the autotrophic production of the endosymbionts (fig.2.4b). Heterotrophic nutrition in corals is achieved by utilizing the crown of tentacles surrounding the mouth. Nematocysts and spirocysts are important in capturing zooplankton prey and protecting the coral from predators (see fig. 2.4 and 2.5a). Epitheliomuscular cells (also known as myonemes) and the subepidermal nerve net provide the polyps with the ability to expand or contract their bodies and tentacles, detect changes in the environment, and communicate with other polyps in the colony. Indeed, food captured in this way by one polyp is shared with neighbouring polyps via the gastrovascular system. Polyp mouths are also directly involved in the exchange of water, food particulates and metabolic waste products between the gastrovascular system and the external seawater. There is also general diffusion of gases and dissolved organic matter across the body surface.

A particular interesting case is the Caribbean atentacular coral Mycetophullia reesi. It captures particulate food by mucus entanglement (Fig.2.5b). Hereby, mesenterial filaments act as surrogate tentacles to emerge through the oral opening, collect the mucus-embedded particulates, and withdraw to the gastrovascular system.^2.20a Other corals also acquire nutrients by harvesting microbes from the water column through mucus netting and indirectly via capture of protozoa that graze on bacteria. Although nematocysts and spirocysts are important in heterotrophic nutrition and inter-species defenses, they seem inefficient in protecting the animal against pathogenic micro-organisms (certain viruses, bacteria, fungi, protozoa).
Since bacterial associations can glean information from the environment and from other organisms, and thereby interpret the information in a ‘meaningful’ way. Making use of advanced communicative capabilities, bacteria lead rich social lives for the group benefit. Doing so, they develop a collective memory, use and generate common knowledge, develop group identity, recognize the identity of other colonies, learn from experience to improve themselves, and engage in group decision-making, an additional surprising social conduct that amounts to what should most appropriately be dubbed as social intelligence. Indeed, such a bacterial colony behaves much like a multicellular organism (comparable to a social community), with elevated complexity and plasticity that afford better adaptability to whatever growth conditions might be encountered.^2.20b Many Gram^NEG bacterial species use quorum-sensing molecules to turn on the expression of a variety of genetic suites (e.g. virulence genes) once the species density exceeds a threshold.^2.20c Thus, unfavorable environmental conditions do favor microbial responses that alter the composition of the MPS-Layer in a way that pathogenic manifestation become established; i.e. expression of virulence genes of microbial associates among this bacterial biofilm and proliferation on such altered MPSL-substrate that ultimately induces so-called coral diseases (see Chapter-IV for a more detailed presentation of this issue).
As indicated above, and in order to better comprehend the dynamics behind this fragile equilibrium, it is important to recall that radical physical and chemical changes occur within the MPSL not only on a daily basis, but also during stress events. Indeed, most coral species use mucus to entrap and cultivate "beneficial" microbial matter and utilize it as an additional food source. Here, the more or less acidic mucus provided by the coral acts as an enriched surface substrate to boost growth of selected microbes. Its noteworthy to mention though that coral mucus is not just used on a microscopic scale; it is also a major nutrient source for many grazing reef-organisms that both consume the prokaryotes and the substrate.^2.21

Micro-organisms contribute through a number of pathways to the total coral energy budget (fig.2.6).^2.22a The provided coral mucus acts as an enriched surface for microbial growth enabling the coral to directly "feed" on them. Sorption of the microbial mat makes sure that their density is kept within the exponential growth phase. Given the optimal growth conditions, microbes are encouraged to transform the mucus with ectoenzymes or aggregation reactions suggesting that the prokaryotic interaction with the biofilm is subtle and finely tuned form of a symbiotic relationship – probably as important as the coral’s algal endosymbionts.^2.22b

Although nitrogen relationships within the MPSL are poorly known, microbial nitrogen fixation is very likely when considering that the matrix does become micro-aerophilic to anaerobic.^2.23 Thus, corals not only “fish” for nutrients (carbon, nitrogen and phosphorous sources) by utilizing both microbes and their metabolites, they also assimilate the newly fixed nitrogen from nitrogen fixing associates and utilize the selective prokaryotic association to protect the coral animal from opportunists (so-called pathogens) by occupying entry niches.^2.25 Recent studies assign the coral’s endolithic community similar properties in that the micro-organisms within the coral skeleton may satisfy 55-65% of the coral’s nitrogen requirements.^2.26a
Chlorophyll pigments associated with Ostreobium result in a green band of freshly fractured coral color (see fig.5.10, Chapter V). As with the above, their nutrients are translocated in the form of photoassimilates and fixed nitrogen. So far most of the research in coral microbiology has been restricted to studying bacteria that are associated with coral pathogenesis. But as demonstrated so far, these are only few aspect of the complex and poorly defined ecological role of bacterial communities. It is therefore essential to deepen the understanding of the microbial composition and the associated processes involving both coral mucus as well as coral skeleton.^2.26b Despite this complex association do corals possess a certain innate immunological capacity. They do so by reacting in a non-specific ability to many potential pathogens. This is of particular interest as any adaptive immunity against pathogenic micro-organisms has not yet been demonstrated elsewhere among invertebrates. Furthermore, little or no antimicrobial activity could be detected in the various species of stony corals tested so far.^2.27 And still, the coral is not victimized as it possesses innate (natural), non-specific abilities to move, shed or expel "pathogenic strains" in several ways. Host defences include (1) physical barriers (provided by the epidermis, i.e. apical cilia on the supporting cells move, shed or sweep trapped particles off the colony surface), (2) chemical barriers (secretions of chemicals, e.g. acids), (3) biological barriers (production of bioactive compounds, e.g. antimicrobial peptides such as makrokines which are similar to cytokines), and (4) ingestion via engulfing amoeboid phagocytes, which lyse invading microbes. The coral’s defenses against microbial infections also utilize inducible components such as encapsulation via phenoloxidase-catalysed melanization, and multi-step processes such as opsonization as well as phagocytosis initiated by lectin recognition (agglutination of micro-organisms renders them easier to phagocytosis) which are consequently lysed by proteolytic enzymes and free-oxygen radicals.^2.28

Autotrophic Nutrition: Food compositions in tropical waters is rather low, thus most shallow water hermatypic reef corals host symbiotic algae in their tissue to complement their diet. This symbiotic relationship is attributed to single-celled plants called dinoflagellates - often referred to as “zooxanthellae”.^2.29 Like any plant, these algae use sunlight (E = h·ν), carbon dioxide (CO₂), water (H₂O) and nutrients (nitrogen, phosphorous, and trace elements) to produce sugars and cellular material. Unlike terrestrial plants, these endosymbionts are embedded in the animal tissue to contribute to the coral’s nourishment. Together they provide the physical framework and much of the primary productivity of coral reefs.^2.30 The paucity of scleractinian families (5 out of 23) among seven genera, which have both endosymbionts and strictly heterotrophic members is an indicator for the relatively long-term-evolutionary stability of photosymbiotic associations. The most ubiquitous of these dinoflagellates to be found among coral animals are those of the genus Symbiodinium.^2.31 It is important to note that each dinoflagellate strain (or species of the algal family Dinophyceae) does have different adaptive capabilities and tolerances to environmental conditions. Members of Dinophyceae have very distinctive morphology and physiology and most of them are nutritional opportunists, capable of photosynthesis but also of using organic foods.^2.32 Free-living motile dinoflagellates are usually found in the dinomastigote stage – a stage in which the cell possesses two flagella and exhibits a characteristic swimming pattern. This is quite different among the endosymbiotic forms. Unlike their free-living counterparts, they are found in the coccoid stage, are non-motile, and lack the characteristic flagella. Obviously, these algal cells undergo a transition as they are phagocytosed into vacuoles within the gastrodermal cells. Specialized recognition patterns on both the dinoflagellate and among the coral animal make sure that they are not digested during phagocytosis.
These symbionts are not only essential to the host in terms of organic productivity (gain the majority of their carbon requirement through this symbiotic association) but they enable the coral animal to contribute significantly to the carbonate framework of reefs.^2.33,
In fact, a major biotic control of the production of calcium carbonate is the rate and form of photosynthetic (primary) produce. Being part of a positive feedback-loop, any increase in photosynthate results in an enhanced calcification rate. On the other hand, the host itself is capable to regulate endosymbiont densities. This is of particular interest in damaged coral tissues. Even though sexual reproduction in dinoflagellates has not been documented so far, regeneration of damaged coral tissue is achieved not only by an induced overall increase in endosymbiont concentrations at the site of injury but also via active transport of gastrodermal cells within the two inter-connecting canals of the gastrovascular system (compare fig.2.4a).^2.34

Photosensitive Accessory Pigments: Apart from the photosensitive pigments within the coral endosymbiont (see below), the coral host animal provides complementary pigments that aid in photo-acustomization of the coral-algal holobiont. Reef-building corals are known for their brilliant colors. These are due to a family of green-fluorescent proteins (GFP) that fluoresce under ultraviolet (UV) and visible light (VIS) with emission maxima at 420-620 nm. These pigments (also known under the generic term ”pocilloporins'') reveal molecular properties that are involved in the conversion of high-intensity UV-radiation into photosynthetically active radiation (PhAR).^2.34a
Thus the fluorescent pigments (FPs) of corals provide a photobiological system for regulating the light environment of coral host tissue. Under low light, FPs may enhance light availability, while under excessive sunlight, FPs are photoprotective. They achieve this by dissipating excess energy at wavelengths of low photosynthetic activity. Thus, FPs enhance the resistance to abiotic TBL of corals during periods of heat stress.^2.34b
Since high levels of light during periods of peak irradiance cause photodamage and photoinhibition in coral endosymbionts^2.34c, it does not come as a surprise that the highest numbers of fluorescent coral morphs can be found in shallow waters. Hence FPs reduce the susceptibility to photoinhibition of fluorescent corals by altering out damaging UV-A and excessive PhAR.^2.34d A significant correlation between bleaching resistance (that is, high tissue dinoflagellate biomass) and the concentration of FPs within the tissue was found.^2.34e White-pigmented regions of tissues, formed by dense layers of FP chromatophores, had 60-100% reflectivity with respect to the highly reflective bare coral skeleton. The most pigmented, and most reflective, parts of colonies – branch tips and colony edges, oral disk/cone and tentacle tips, which on polyp retraction form a sun-screening polyp ‘plug’ - correspond to known areas of highest cell division and areas immediately above reproductive organs. Under high light, polyp contraction leads to denser concentration of tissue FPGs and cytoplasmic FPs, forming a thicker and a quasi-continuous FP layer; this layer acts as an effective sunscreen. Since photosynthesis of dinoflagellate is vulnerable to both UV and high levels of PhAR. in high-light-acclimated corals, FPs are localized above the endosymbionts to screen them from excess sunlight. In shade-adapted corals FPs are localized endodermally among or below the layers of endosymbionts. While accessory pigments in dinoflagellates can dissipate excess PhAR as heat, FPs can dissipate excess light energy through fluorescence and light scattering by transforming absorbed UV-A radiation to longer non-actinic wavelengths through fluorescence. Hence, FPs supplement screening of UV-radiation of mycosporin-like amino acids. By screening chlorophylls and peridinin from high levels of solar radiation and by absorbing UV-A, FPs thereby decrease the likelihood of irreversible photoinhibition, photooxidation and subsequent coral bleaching. ^2.34e
The Endosymbiont: As shown in figure 2.8, the dominant dinoflagellate feature evident on an ultra-structural level is the nucleus revealing the permanently condensed chromosomes (dinokaryon).^2.34f Dinoflagellates reside exclusively in membrane-bound vacuoles within the gastrodermal cells.
As with any plant, these algal cells undergo photosynthesis under illuminated conditions and exchange nutrients and waste molecules with the surrounding polyp cells. Besides their obligate pigments such as chlorophylls a and c, they also contain accessory pigments (such as dinoxanthin, diadinoxanthin, β-carotene and peridinin);^2.36a together they serve to cope with the drastically varying light conditions in aqueous habitats – especially to boost absorption efficiencies with increasing depth (fig2.7c & fig2.7d).
In order to protect themselves from over-exposure on shallow-reefs (see Radiation, chapter-III),^3.62c the symbiotic algae of reef-building corals exhibit protective properties of ultraviolet (UV) absorbing compounds. Among such UV-b protective molecules are mycosporine-like amino acid (MAA) and scytoenmin; metabolites found in a variety of marine organisms. These compounds have absorption peaks in the UV (wavelength absorption maximum λ ranging from 310 to 360nm) and therefore intercept damaging photons before they reach DNA and other cellular components.^2.36b For this purpose, concentrations of MAAs of A.microphthalma tissues for example at 1m depth are significantly higher than those at 20 and 30 m depths. MAAs are one of nature’s sunscreens, with 19 structurally distinct MAAs presently identified in marine organisms (the skeletal configuration of this molecule is shown in fig.2.7e). Furthermore, experiments have shown that Symbiodinium cultured at high temperatures has lower concentrations of MAAs than cultures grown at lower, unstressful temperatures – indicating that MAA is synthesized within the endosymbionts and forwarded to the coral host.^2.36c

The discrete antenna complexes within both the chlorophylls and the accessory pigments molecules are embedded in sac-like membranous structures (thylakoid) of the endosymbiont, and convert sunlight into energy (carbohydrates). Since the energy level to synthesize carbohydrates from water and carbon dioxide is very high the only way to achieve oxygenic photosynthesis is to split this task into two intermediate steps, i.e. via two separate photosystem complexes (PS-I & II, see fig.2.8).^2.38
ATP is produced via photolysis of water during the 1^st light-reaction within the photosystem-II (photo-phosphorylation):

It is important to remember that along with the increasing proton gradient, a complementary electron-density is established within the thylakoid membrane. The excess concentration of negative charges is routed through the electron-transport chain and used to activate NADP. On the other hand, the proton gradient obtained during the light reaction from both photosystems is used during the dark reaction to enzymatically synthesize glucose from CO₂:

Corals exposed to different light regimes are capable of photoacclimation. This is a process used to increase the production of photosynthate with decreasing irradiance. Thereby the concentrations of the light-harvesting pigments (chlorophylls-a & -c and peridinin) of the endosymbiotic algae are increased, while at the same time photoprotective pigments like dinoxanthin and diadinoxanthin, and β-carotene are decreased (i.e. typical for shallow-water corals).

Photoinhibition on the other hand, is a protective mechanism to shield the algae from excess irradiance (fig.2.8b). It can be achieved by (1) modification of colony morphology, (2) behavioural responses such as expansion and contraction, (3) chemical adjustments of concentration of accessory pigments, (4) activation and increase in levels of antioxidant enzymes present in both coral and algae that also protect the coral from oxidative stress.^2.41 It was shown that thermal stress in endosymbionts disturbs the Mehler-Ascorbate-Peroxidase (MAP) cycle so important in the absorption of excess electrons (prevents an accumulation of light-generated reductant), and an overshooting pH-gradient (that otherwise would result in increased dissipation of heat). It is thought that during heat-stress events the electron flow to NADP-reductase, that otherwise converts NADP to NADPH is blocked. This blockage causes not only an increased electron flow to the MAP cycle, but also a drastic increase in charge separation within PS-II that exceeds, under high light, the capacity of electron flow though the MAP cycle. Eventually, the resulting increase in ΔpH across the thylakoid membrane initiates a photo-protective stress reaction, in which energy is dissipated in the form of heat.^2.42

Although light is essential for the high productivity of coral reefs under normal conditions, higher than normal temperatures render light to become a liability.^2.44 Essentially, increased light levels boost the light reactions to levels in which the build-up of potentially harmful products such as various free radicals, are favored. Under normal conditions these radicals are detoxified by several enzyme systems (e.g. superoxide-dismutase & ascorbate-peroxidase), or by oxygen radicals (e.g. •O₂^-, H₂O₂, •OH^-) ,^2.45 which are also the main agents in the defence against opportunistic microbes.^2.46 Thus, if the enzymatic regulatory mechanism is hampered, these hyper-reactive components rapidly turn against the coral cells and cause oxidative damage. Unfortunately, abiotically induced tissue bleaching does not just interrupt the pathway to the dark reaction (see TBL, Chapter IV), but it results in the buildup of oxygen-radical that denaturate the enzyme mechanisms that are usually involved in detoxification of these radicals. Eventually and in order to avoud self-intixication, the prolonged build-up of toxins forces the coral animal to expel their endosymbionts (fig.2.9a).

If such stress events do not persist for extended periods of time, the coral is able to re-acquire free-living dinofagellates to become again fully functional (algal cells are phagocytosed into vacuoles within the gastrodermal cells, but are not digested).^2.47 In order to reach pre-bleached endosymbiont densities, the incorporated dinoflagellates multiply by mitotic division.^2.48 From this perspective, bleaching can be considered an interim period where switching between Symbiodinum taxa that have different thermal optima seems to occur, which may lead to improved host survival.^2.49a

Adaptive Bleaching Hypothesis (ABH)^2.50 was initially conceived to explain the paradox of reefs seeming robust in the long, but fragile in the short term. Here, adaptation implies the modification of the organisms or its parts in a way that makes it more fit for existence under new environmental conditions. Thereby the ABH neither involves speciation nor extinction, but rather implies the genetic alteration as well as composition of the holobiont, and occurs over very short timescales (within the life time of the partners). Concerning the endosymbiontic associations, this is a complex process and unlikely to happen in the ecological time frame of a bleaching event. The ABH can be envisioned as a rare stochastic process operating along a continuum (of two environmental end states). One is a discrete change in environmental state (e.g. major changes in current patterns due to gradual climate shifts), while the other one consists of rapid oscillations around a stable baseline of environmental conditions.
When considering global climate change, the ABH has the potential to become an essential key in the long-term survival of coral species. Thus, catastrophic bleaching may merely represent a temporary extreme end of that continuum, which includes natural fluctuations in symbiont standing stock over seasonal timescales. Initially, what seems a maladaptive response to trauma (breakdown of the host-algal symbiosis) turns into an alternative strategy to overcome photoinhibition.

Corals that survive an abiotically induced bleaching event may have temporarily expelled their endosymbionts, but eventually phagocytize free-living algae and regain normal densities as environmental conditions normalize (the argument of tissue bleaching is picked up again in Chapter-IV). If genetically distinct strains or species of endosymbiont are incorporated or “residual algal polulation” remained within the coral, “rebrowning” is a process by which a change in the genetic composition of the algal population may take place.^2.49a
Indeed, some decades ago only a few types of Symbiodinium have been documented, while today the distinctions rose to 50-60+ types and still keep rising. Several particular Symbiodinium sub-genera or clades inhabit these reef ecosystems. One of these groups, referred to as clade C, dominates corals and their relatives throughout the tropical Indo-Pacific (fig.2.9b).^2.53a Even though clades A, B, C and D are more evenly apportioned across Caribbean invertebrate communities, those of clade B are among those most frequently encountered. The unusual prevalence of clade H in the Caribbean and the eastern Pacific may be a consequence of isolation that began with the final closure of the Central American Isthmus.^2.53b Accordingly, the high-latitude clade F is found in more temperate regions (i.e. in the North-Western Pacific such as in Alveopora japonica).

There is ample evidence that such shifts in the ratio of algal genotypes in polycladal symbioses do occur. However, concerns remain as they are ultimately restricted by their genotypes, i.e. an upper thermal tolerance set by both the host and their partners.^2.53c It remains to be seen weather coral hosts are able to modify the type of endosymbiont fast enough to keep pace with the rapid changes in environmental conditions. A remark that clearly underlines the scarce knowledge about the algal-coral relation. There is an urgent need to document symbiont diversity, the factors governing symbiont community change, to investigate the mechanisms of symbiont acquisition, the diversity of free-living Symbiodinium and to analyze the functional diversity of Symbiodinium, their bleaching resistance as well as their distributions.^2.54

Cost and Benefit of the Coral-Algae Symbiosis: The balance between photosynthetic production and the metabolic cost of maintaining the algae includes mechanisms to cope with high oxygen tension and possible regulation of endosymbiont growth rates. Average densities oscillate at around 1-2·E⁶/cm² of coral surface area. It is assumed that this range represents the optimal algal density that balances the benefits and costs of this symbiotic relationship (i.e. the net return to guarantee the survival of both organisms).^2.55

The benefits for the animal consist in a regular supply of carbohydrates, which aids considerably to the coral’s metabolic requirements (increased rates of growth, calcification, reproduction). At the same time endosymbiotic activity supports in the conservation of nutrients, while toxic compounds are sequestrated by the algae. The costs for the animal includes the regulation of algal growth, construction of peri-algal vacuoles (provision of a good habitat, see fig.2.10), establishing defenses against high oxygen tension, light and UV, as well as creating mechanisms to reject foreign or excess algae.^2.57a Yet, this symbiotic relationship has a major drawback: it restricts the coral animal to the narrow circumtropical band within the photic zone of the littoral.

From the alga’s perspective though, the benefits include a constant supply of CO₂ and nutrients from the host, protection against damaging UV-radiation, to a certain degree from predation, and maintenance of a high population of a single genotype under uniform environmental conditions. The costs on the other hand include the translocation of a significant amount of carbohydrates to the host, regulation of its growth by the host (slower compared to the free-living form) and expulsion when population densities become too high or unfavorable under altered environmental conditions.

The “economic” benefit of this partnership can be encircled by an increased competitive advantage for space on the reef, resource partitioning and due to the accreted carbonate skeleton, some mechanical protection against wave motion – not to forget their essential role within the trophic pyramid. On the other hand this partnership restricts the coral holobiont to narrow but optimized environmental fluctuations, particularly in terms of temperature, light, and sedimentation conditions. Such narrowed ranges of tolerance highlight the stenobiotic environmental conditions that prevailed over long times in establishing the evolutionary relationship necessary for their survival.^2.58

Reef Accretion in the form of Calcification: The world’s oceans are not only a huge buffer but also the only re-distributive means by which dissolved compounds are cycled across the globe. Coral reefs are dynamic systems, producing limestone at the rate of 0.4-2·E³ tons per hectare and year, thereby significantly influencing the chemical balance of the world’s oceans. Thus, six ions make up more than 99.4% of the salts (by mass)^2.59 that are dissolved in seawater: sodium (Na⁺), magnesium (Mg⁺), calcium (Ca²⁺), potassium (K⁺), chloride (Cl^-), and sulfate (SO₄^2-). Ocean water is also slightly basic and buffered against changes in its pH, which oscillates around 7.5-8.2 (average 7.8). Carbon Dioxide (CO₂) is the major agent regulating the buffing capacity within the marine habitat. Actually, if the pH of seawater would vary appreciably, many marine organisms would die.
Roughly half the calcium (Ca²⁺) that enters the sea each year around the world (from pole to pole) is taken up and temporarily bound in coral reefs. With each atom of Ca²⁺, a molecule of CO₂ is also deposited. The gross fixation of CO₂ is estimated on the order of 700·E⁹ kg carbon per year.^2.60 Both regeneration capabilities and the accretion of the calcium-carbonate (CaCO₃) skeleton are mainly achieved through the energetic contribution provided by endosymbiotic algae.

Since Calcium-ions (Ca²⁺) are readily available in the marine environment (1.17% by mass percentage), the precipitation reaction merely depends on the dissolved bicarbonate concentration (HCO₃^-) - its mass-percentage oscillates around 0.5%. Due to the optimised bicarbonate pool in seawater it requires little energetic effort by marine organisms to shift this balance toward the solid carbonate end of the equation (fig.2.11). It is thus not surprising that many marine organisms (from the bacteria to vertebrates) utilize these two building blocks to enhance their chance of survival.

As outlined in fig.2.11, the chemical reactions involved are the manifestation of a dynamic equilibrium with changes in bias from educts to products and vice versa taking place in continuation. This is particularly important since less carbon dioxide can be dissolved in tropical warm waters than in ice-cold waters. An increase in greenhouse gas levels (e.g. partial pressure of carbon dioxide, pCO₂) coupled with storm-activity (strong winds and heavy seas) dissolves more CO₂ into the ocean thus raising the bicarbonate concentration of surface waters. At a first glance, elevated pCO₂ levels seem to provide more educts for the final precipitation reaction, but a closer look reveals that bicarbonate as a week acid (slightly pushes the surface pH towards the acidic regime), making it harder for the organisms to work against a steeper precipitation gradient. Under ideal conditions (optimal light, normal pressure, and moderately elevated temperature) the following stoichiometric reactions take place (fig.2.12):

Although dissolved Mg²⁺ is three times more abundant in seawater than Ca²⁺, the resulting magnesium-carbonate (MgCO₃) constitutes only a tiny fraction, i.e. 0.1-10% of the total precipitate.^2.64 The remaining 90-99% consist of aragonite rather than calcite. The former is not only structurally stronger than the latter, but aragonite readily precipitates in warm seawaters, while it is more soluble in cold water (compared to freshwater).^2.65 Aragonite is characterized by a needle-like crystalline structure (orthorhombic crystals with a thickness of 10μm and lengths up to 100-500μm, see fig.2.12b). Calcite on the other hand forms rhomobohedral crystals. While aragonite is the most common CaCO₃ precipitate produced by marine organisms (and also a lot easier to dissolve), calcite predominates ancient limestones, thereby making such abiotically induced precipitation reactions an important reservoir of CO₂.
It is still not quite clear why corals do become involved in carbonate precipitation in the first place. Several theories have been established; among them one can find the CO₂-utilisation-theory (proton activity decreases as CO₂ is consumed by endosymbionts), HCO₃^- -theory (coral cells produce OH^- -ions to keep the cytoplasmic pH at constant levels), Organic Matrix theory (maintaining cytoplasmic Ca²⁺ levels at constant levels favoring precipitation), Carbo-Anhydrase theory (enzyme-mediated precipitation reaction), micro-organism induced theory (certain micro-organisms can increase the precipitation efficiency). The question why especially the aragonite-morphotype is preferred has been evaluated in five different hypothesis’; i.e. Goreau-hypothesis (see above, fig.2.5b), nucleiation-hypothesis (crystal growth induced via maternal minature inoculation crystal); crystal-poison-hypothesis (use of phosphate ions to control skeletal morphology); matrix-hypothesis (fast-growing R-strategists precipitate a weaker skeleton than slow-growing K-strategists); urea-hypothesis (urea used as a proton acceptor facilitating the precipitation reaction).^2.66a
Current evidence suggests that the organic-matrix-mediated mineralization is a combination of all these theories, by which the animal ultimately constructs an organic framework that is induced by nucleation and followed by gradual accretion based on this crystallographic skeletal micro-architecture. It also remains unclear to what extent the filamentous algae present in the tissue-skeletal interface contribute in this process (see Mycetophyllia reesi fig.2-12b). While the algae undoubtedly aids in the separation of tissue and skeleton, areas without algae have also been documented. ^2.66b The accretion of the carbonate framework is primarily a function of endosymbotic activity, availability of Ca-ions, and temperature. Since aragonite is more soluble in seawater than calcite, redissolution of the former directly determines re-crystallization into the latter, which is a function of this rate of supply and found as accumulations on the ocean floor. Deeper water masses are generally undersaturated with respect to aragonite and calcite, and thus dissolution occurs both in the water column as well as on the sea-bed.

The degree of undersaturation is not only controlled by the pCO₂ of deeper water masses, but also by the amount of organic matter oxidized, and again temperature. Fig.2.13a illustrates the relationship between the degree of aragonite and calcite saturation in seawater of both the Atlantic and the Pacific. Ca-precipitation is depth (pressure) dependent. At depths less than 300m, the reaction tends to favor the precipitation reaction; equilibrium is reached at around 300m, whereas beyond this depth more CaCO₃ is dissolved than precipitated.^2.67a The aragonite/calcite compensation depths are deeper at the equator, where the supply of carbonate material is greater.
There is clear evidence that the carbonate equilibrium of the oceans is shifting in response to increasing atmospheric CO₂ concentrations. Potential long-term impacts of anthropogenic CO₂ on the calcite and aragonite saturation state of the oceans have been discussed in detail by various authors. Past, present, and future aragonite saturation horizons have been modeled based on historical data and IPCC “business-asusual” CO₂ emission scenarios. Fig.2.13b shows a comparison of the pre-industrial, 1994, and 2100 saturation horizons for the Atlantic and Pacific based on such modeling results. Modeling efforts for surface waters indicate significant reductions in aragonite saturation state of the tropical and subtropical oceans over the 21^st century. These conditions will have significant impacts on the ability of coral reef ecosystems to maintain their structures against the forces of erosion and dissolution.^2.67b Indeed, as CO₂ rises and makes the ocean more acidic, it reduces the concentration of carbonate ions in the water. This makes it much harder for corals to build their limestone skeletons. Repeated experiments have shown a drop in skeletal growth rates of least 30% in the next hundred years.^2.67c

Coral Reproduction:
As with any living organism reproduction is vital if species intend to persist for future generations. Reproduction though not only is hampered or stopped altogether by biotic and abiotic stressors (sedimentation, diseases, pollution, etc – see Chapter III) the same can be achieved when reproduction through recruitment fails.^2.68 Corals are able to produce offspring both sexually and asexually. It is important to note that some corals, especially massive ones such as Porites behave more like K-strategists when compared to the "weedy" Acropora species that resemble much more R-strategists.^2.69 Asexual reproduction is performed when initial population densities are low and gametes of opposite sex and different colonies have an unrealistically low chance to "see" each other, thus sexual reproduction sets in once corals form a more or less dense carpet throughout the reef.

In asexual reproduction, the parental coral produces exact copies of itself (clones). This process in which new polyps are constantly developed is commonly known as budding. As shown in see fig.2.14a, additional polyps arise from two distinct processes. One can differentiate between the division of a polyp into more or less two symmetrical halves (intratentacular budding), while the other pathway develops a new mouth with a separate tentaclular crown in the space between two adjacent polyps (extratentacular budding). As the newly formed polyps remains attached to the parent colony, both types of reproduction result in the gradual growth of the colony (increase in size). If these polyps / buds become detached from the parent colony they ultimately will give rise to new colonies. This process is also known as polyp bailout.

Here polyps actively detach from the parent colony (exposing the underlying coral skeleton) and drift away through the water column, aided only by their cilia which cover the outer surface, until they come into contact with the appropriate surface for settlement.^2.70 Fragmentation of the parental colony represents a similar and frequently encountered variation of asexual reproduction. It is most prevalent among finely branched or plated corals. Fragments that fall onto a solid bottom may fuse with the substrate and continue to grow through budding.

Borehole analysis of massive hermatypic corals have revealed periods of growth, dieback, and regrowth. This is of particular interest especially in century old colonies. In such cases it seems that asexual reproduction is not only achieved via budding, but also via a process known as parthenogenesis (i.e. unfertilized eggs mature into ciliated planulae larvae, that are able to drift away, eventually settle on a suitable substrate and ultimately giving rise to a new colonies. Although the variations described so far are of regular occurrence, they all have some major drawbacks, which include an unaltered genetic code accompanied by the impossibility to improve both genotypic and phenotypic expressions, leading to a more or less static (rigid) level of fitness as well as a reduced adaptive capacity in responding to environmental challenges. Therefore such clonal populations do not possess the genetic variability to face a permanently changing environment and thereby become increasingly vulnerable, which ultimately limits their long-term chances of survival.^2.72

Although asexual reproduction has the least risk and is 100% successful, sexual reproduction is the way to go to overcome limitations encountered in clonal reproduction. The most obvious advantages can be summarized as follows: offspring have the chance (1) to profit from successful parental properties, (2) to inherit a new genetic features not present in the parental genotype, (3) favored by positive epistasis,^2.73 and thereby (4) reducing species vulnerability. Even though recruitment success in sexually reproducing species can be quite low (compared to cloning) sexuality makes use of the entire genotypic spectrum available within a species, thereby minimizing the risk of extinction as still a few of the offspring will survive to eventually reach sexual maturity (compare fig.2.2). This is especially important as environmental conditions never remain the same – they are in permanent flux, always changing and thus forcing the animal to constantly readapt itself; an adaptive response commonly known as the “Red Queen Effect”.^2.74

Sexual reproduction involves the merger of germ cells (egg and sperm) of different parental colonies with similar genomes and eventually ensures that intra-species diversity is maintained. Contrary to the diploid character of parental somatic cells, germ cells are the result of meiosis and thereby contain only one member of each homologous pair in its nuclei. Thereby, the increase in genetic recombination is made possible in a process known as crossing over. Meiosis works in two phases:^2.75a While the chromosomes are paired in meiosis-I, enzymes randomly break the DNA molecule in each homologue, switch corresponding regions of each chromosome (the actual crossing over), and then attach them to new chromosomes of mixed ancestry of the diploid cell. During the separation phase of meiosis-II, homologous chromatids split. The haploid character of the germ cells is only attained once separation of the chromatids took place and cytokinesis is completed. Now each progeny cell contains only one member of each homologous pair in its nuclei. Female gametes (eggs) are large, more or less mobile, while the male gametes (sperm) are small motile cells.

Since the random fusion of egg and sperm (fertilization) of two different parents further increases genetic variability among populations, causing the hereditary information from both parents to unite, it creates a single cell with a genetically unique combination of genes and chromosomes. The resulting zygote (fig.2.14b) is again diploid and fitted with a homologous pair of chromosome. Together, both effects (crossing over and fusion to a zygote) lead to enhanced survival of species.

Species that either produce sperm or eggs are said to be gonochoric (also known as the dioecious) and includes approximately 25% of the coral species studied so far (among them genera like Porites and Galaxea). The identification of separate sexes in corals is sometimes confused by the fact that it takes eggs longer to develop than sperm. On the other hand, individual species capable of producing both eggs and sperm are said to be hermaphroditic (fig.2.14c). Hermaphroditism is particularly favorable in small populations.

A narrower definition is applied when the production of eggs and sperm take place at the same time, in which case the species are grouped as simultaneous hermaphrodites. Here gamete bundles typically consist of 9 to 180 eggs embedded within a mass of sperm. The majority of species studied so far have been identified as simultaneous hermaphrodites (most acroporids, faviids, and some pocilloporids). Two separate cases are discriminated among sequential hermaphrodites: Protandry is a frequent occurrence among many reef organisms, in which case species develop into a functional male first, and only later in life to express female reproductive organs, while protogyny outlines those cases where gonad development occurs in the reversed order. Only few species so far have been found to be sequential hermaphrodites (e.g. Stylophora pistillata and Goniastrea favulus).^2.76

There are two different modes of reproduction that influence many aspects of coral ecology; it regards the transfer of symbiotic algae to the larvae, and larval competency - that is, the capability of settlement and metamorphosis (see fig.2.13).

Brooders (or sometimes also referred to as planulators) include species that fertilize eggs with sperm internally, with the embryo developing into the planula-stage inside the female coral polyp. Cytoplasmic extensions of gastrodermal cells containing endosymbiotic algae invade the egg plasma,^2.77 and thereby provide a full complement of endosymbiotic algae from the parent colony.^2.78

Development of the brooded larvae is slow and takes months to complete, often falling together with the maturation of next generation of eggs.^2.80a As a result, brooded larvae are generally larger than spawned larvae, making the released planula immediately competent. Brooders are found to represent only about 15% of the coral population studied so far (e.g. Caribbean agariciids and poritids, and others.)^2.80b

Broadcasters: External fertilization is the key element among species releasing bundles of egg and sperm into the water column. Spawned gametes are positively buoyant, causing the bundles to aggregate on the water surface and to break open where the gamete populations merge to form zygotes (fig.2.15b). Sperm concentrations of 10.6/mL have been found to be optimal for fertilization. Many coral species mass spawn. However, the triggering factors of seasonal mass spawning are not totally clear.
Over the last years literature on coral reproduction schedules has expanded to include localities, such as the Solomon Islands, Singapore, Palau, the Philippines and Kenya.^2.79f Surprisingly, the duration of the coral spawning season varies considerably among these regions. Therefore, there are a multitude of questions awaiting an answers: i.e. why does the coral spawning season vary regionally? Is the duration of the spawning season driven by an environmental factor? Is an extended spawning season the default system? Or is there a natural drift towards asynchrony in tropical systems?
Coupling gamete release with environmental conditions has been assessed on at least three temporal scales:
i) Nocturnal gamete release is required for the majority of broadcast spawning species (although Porites and Pocillopora may spawn in daytime). During mass spawning, many species stagger their release times through the evening; that is in southern Japan and Palau for example, most mussids (Lobophyllia spp.) spawn early, at 18:30, followed by Montipora and Acropora species around 19:00–20:00, faviids at 20:00–21:00; and fungiids as well as Porites spawn later at 21:00–22:30. Such staggering may facilitate the maintenance of species boundaries.
i) There is no globally consistent relationship between lunar phase and the timing of coral spawning, because some coral species spawn at full moon in one locality and at quarter moon in an adjacent locality.
i) While the light of the moon may play an important role in the release of gametes, it was also observed that gamete release is closely linked to the time of the year and evolutionary cues that drive this process.^2.81d
The literature contains abundant general statements and possibilities relating marine spawning to seasonal proximate cues, including temperature, the lunar cycle, the amount of rainfall and solar insolation.^2.81e Coupling coral reproductive schedules to optimal temperature (stenobiotic window ranging from 28 to 30 °C) was unquestioned for years, if not decades.^2.79e Most convincing was the strong evidence from the Great Barrier Reef (GBR) that showed spawning on near-shore reefs in October, when the water temperatures were approx. 28°C, and spawning on mid-shelf reefs one month later, when the water temperatures reached identical values. However, localities near the equator have a narrow temperature range, therefore it would seems highly unlikely that corals in the tropics have synchronized spawning patterns. van Woesik et al. (2006) already showed a strong positive relationship between mass spawning in the Caribbean and maximum insolation (or a near-zero solar insolation derivative; i.e. w hen the rate of change in solar insolation is near zero).^2.81a Solar insolation is the amount of electromagnetic energy incident to the surface of the earth (kW·m^-2·day^-1, see Fig. 2.15e) in the range of 300–5000 nm, or at least the photosynthetically active radiation part of the spectra ranging from 400–700 nm utilized by the endosymbiont, while the other regards sea-surface wind intensities (see Fig. 2.15d).^2.81a. Although gamete release in the Caribbean coincided with temperatures between 28 and 30°C, the rate of temperature change was a poor predictor of spawning. A negative rate of change in solar insolation (i.e. the concave-down derivatives) provided the best predictor of gamete release.
Coral spawning in Western Australia has now also been observed twice a year, both in the Austral autumn and more recently in the Austral spring. These biannual spawning modes correspond with solar equinoxes, and are no different to biannual, multi-species spawning in Palau and biannual spawning of three Montipora species on the GBR. Therefore, the genetic legacy hypothesis may play a minor role, since insolation cycles explain most of the forcing. Support to this view comes from Falkner & Falkner (2006), who assign the coral holobiont the capability of processing information by means of interconnected adaptive events.^2.81a. Adaptive events are physiological processes that are characterized by two opposite manifestations, namely adapted states and adaptive operation modes. Thereby, the adapted state is the outcome of former adaptations that has been acquired during a “learning experience”, for example, to elevated solar insolation events that ultimately guided the emergence of the new site-specific adapted state. For this purpose adaptive events had to be considered as elements of a communicating network, in which, along a historic succession of alternating adapted states and adaptive operation modes, information pertaining to the self-preservation of the organism is transferred from one adaptive event to the next: the latter “interprets” environmental changes by means of distinct adaptive operation modes, aimed at preservation of the organism. The result of this interpretation is again leading to a coherent state that is passed on to subsequent adaptive events in the organisms life and epigenetically to successive generations.

Seasonal mass spawning does vary regionally, both in timing and in duration. van Woesik (2009) proposes that corals may couple gamete release when winds are light; i.e. that regional wind fields are the corals’ ultimate reproductive proxy.^2.81b. Coral spawning outside calm periods is most likely autopoietically selected against because gametes would be lost from the reef systems, especially in rather isolated locations throughout the Indo-Pacific. Indeed, by tightly coupling gamete release to calm periods would be particularly advantageous on isolated reefs and in locations where wind fields are rarely calm. Likewise, regions with long calm periods would experience extended reproductive seasons. Such conditions have considerable selective advantages, facilitating fertilization, larval retention and local recruitment.^2.81b
Within a 24-hour period, all the corals from one species and often within a genus release their eggs and sperm at the same time. This occurs in related species of Montastraea, and in other genera such as Montipora, Platygra, Favia, and Favites. Due to pre-mating barriers, hybridization (self-fertilization) is infrequent. Sperm do not readily fertilize eggs from the same colony until 6 hours after release, and even then observed rates of self-fertilization are less than 10%. The same eggs treated with sperm from another colony of the same species demonstrated fertilization rates of 70-100% within 2 hours of gamete release.^2.81c Gametes remain viable and achieve high fertilization rates for up for 8 hours after spawning, thereby increasing the change of intraspecies fertilization.^2.82a

During the mass-bleaching event in 1998, an unusual spawning event was documented on Mirihi (Ari atoll, Maldives). As this was an unusual event for this area and time of the year, the question arose as to the origin of the coral larvae. Among long distance larval transport, a fairly uncommon hypothesis was proposed. Loch et al., came up with the "emergency mass-spawning" event of local scleractinia.^2.82b In the absence of the southwest monsoon, gonad maturation was enforced leading to mass spawning just prior to the bleaching event. Since settlement competency of some species extend to several months, the maturing planulae could have played a predominant role in recolonising Maldivian reefs in the post-bleaching period .
But the fact that gametes and zygotes float at the water surface makes them more vulnerable to the effects of pollution. Contaminants (like oil, polluted freshwater runoffs, etc.) are found at highest concentrations at the ocean surface. Thus, fertilization rates and reproductive success of corals can be seriously hampered by chemical contaminants as these easily interfere with chemical recognition patterns between gametes.^2.83 Regardless of brooders or broadcasters, a certain population density among species must be guaranteed in order to achieve successful reproductive events. Otherwise, population densities of sexually reproducing species that fall below a given threshold level loose out as gamete of opposite sex don’t “see” each other any more (a process known as the Allee effect), leaving the diluted gamete populations unable to merge and to become a zygote.^2.84

Upon successful fertilization, followed by cleavage, the ciliated planulae-larvae become negatively buoyant, and attempt attachment on a suitable substrate to found new colonies on reefs close by, or enrich reef diversity hundreds of kilometers away. As with the floating pollutant issue mentioned above, here an excessive sediment load can likewise act as a barrier preventing coral larvae from detecting the chemical signals from the preferred settlement substrata (e.g. coralline algae).^2.85 By way of being asexual for at least part of their life cycle, sexual reproduction is fortunately not as critical for the coral’s short-term survival. However, it is crucial for the hundreds of thousands of coral-dependent species that are highly dependent on it. Corals may be the least prone to extinction, being able to persist at low density until conditions improve.

As is the case with brooders, some broadcaster populations transfer maternal symbiotic algae into or onto the eggs. Those juvenile corals on the other hand that originate from broadcast-spawning scleractinians, which did not inherit parental endosymbionts, must obtain them shortly after settlement from free-living algal populations. Here, acquisition is facilitated by positive chemotaxis of motile dinoflagellates toward the juvenile coral.^2.86 The indirect acquisition of endosymbitic algae has a major advantage. As illustrated by the ABH, it has the potential that colonization of the juvenile coral is achieved by different algal strains, which are genetically distinct from parental endosymbionts.

Please proceed with Chapter-III (Reefs in Flux, Eutrophication, A/biotic Stressors mediated by human activities)