The pattern of change of the photosystem II (PSII) effective quantum yield (ΔF/Fm’) as a function of the variation in light exposure is correlated with the dynamic photoinactivation of PSII reaction centers and induction of photoprotective mechanisms to dissipate excess excitation energy27 − 29. Differences in ΔF/Fm’ at the end of the diurnal cycle when the light exposure was increased or reduced, reflect differences in the accumulation of photoinactivated PSII reaction centers arising from disparities between the rates of photodamage and repair of the photosynthetic apparatus in the zooxanthellae in hospite. The kinetics of the PSII half-time (t1/2) indicates that the energetic cost of repair of the photodamaged PSII reaction centers for optimizing the algal photosynthetic performance is also variable and mediated by light exposure. This has relevant ecological implications as it can limit the translocation of photosynthetic usable energy to their coral host. This assumption is supported by evidence that the continual replacement of proteins required for the re-assembly of PSII reaction centers can be the largest single contributor to the costs of maintenance in primary producers42,43.
The consistency of the productivity-biodiversity model tested here, despite local differences in reef geological history, environmental conditions and level of diversity, indicates that much of the variation in coral species richness along depth gradients is driven by changes in the fractional contribution of photosynthetically fixed energy by the symbiotic algae to their coral hosts. These findings provide strong support to the occurrence of a productivity-biodiversity relationship in reef-building coral communities similar to that widely acknowledged in communities across terrestrial environments5,6,23. Furthermore, this relationship highlights the fundamental role of primary productivity by the endosymbiotic algae in the structure of coral reef communities. The lack of prior support for the productivity-biodiversity relationship in coral communities12 arise from unclear definitions of the actual energy physiologically available to the coral animal (e.g., solar energy), ignoring key physiological processes that constrain the photosynthetic activity of the zooxanthellae. This contradiction illustrates the difficulty of actually measuring gradients of usable energy available to organisms in studies of productivity-biodiversity relationships and choosing the energy-related variable that best explains species richness variation according to the system studied5–7.
Although coral richness followed a positive relationship with the photosynthetic usable energy supply, the productivity-biodiversity relationship is reflected as a unimodal, humpbacked curve with depth whose shape and mode localization are highly influenced by the water optical properties (i.e., local Kd). The overall humpbacked shape of the curve results from the non-linearity between depth, light availability, and the photosynthetic activity of the zooxanthellae. The increasing and decreasing phases of the humpbacked species-richness curve with depth result from two different processes that can limit the energetic output of the zooxanthellae and, thus, the coral holobiont performance. In deep, low-light environments (the increasing phase of the richness curve), the deprivation of light-energy results in a deficit of photosynthetically fixed carbon that can be translocated to the coral animal. In contrast, in shallow, high-light environments (the decreasing phase of the curve), the increased costs of maintenance of the photosynthetic activity while photosynthesis is fully saturated limit the amount of photosynthetic usable energy that can be translocated to the coral host. This condition is coupled with a strong selective pressure exerted by intense light in shallow habitats, including high levels of UVR 44,45. At intermediate irradiance, the energetic output of the zooxanthellae and the coral holobiont performance are predicted to reach their maximum potential, which can lead to reduced rates of species extinction and increased biodiversity5. The contrasting patterns observed in the productivity-biodiversity curves by location and the relationship between the depth of maximum richness and the local Kd illustrate the essential role of the water optical quality on zooxanthellate coral communities. This role is not only limited to defining the lower depth distribution41, but also, as determinant of depth-related biodiversity patterns. It is worthy to note that the water optical quality can be highly variable in some sites because of the influence of particular meteorologic and oceanographic conditions3,46, and that a single Kd may not represent the complex dynamics of the underwater light climate. Understanding this variability, although crucial for estimating the spatial-temporal variation in benthic primary production4,19, is beyond the scope of this study.
Zooxanthellate corals display contrasting photoacclimation responses, coral cover, colony morphologies and genetic richness along depth gradients32,47−53, which collectively suggest that coral species occupy different light niches. Particular colony geometries that optimize light capture and photosynthetic energy acquisition seem to be selected for maximizing the energy output at the colony level in specific light habitats47,53. Shallow-water corals, for example, adopt complex morphologies (e.g., branching and corymbose) to increase self-shading while maximizing the photosynthetic output, whereas deep-water corals adopt flattened morphologies to maximize light capture48–51. These patterns suggest that a driving force of colony morphology could be determined by a compromise between maximizing the photosynthetic production while minimizing the energy expenditure in photorepair. Additionally, the association with symbionts with distinctive photoacclimation potential can allow corals to cope with contrasting light climates along depth gradients and within colonies32,54−57. The location of maximum translocation of photosynthetic usable energy at intermediate irradiance may promote a more widely available specialization space and evolutionary innovation in that particular habitat with regard to colony geometry and symbiotic associations, allowing more coral species to coexist8. Conversely, the variety of viable specializations that emerge from combinations between colony morphology and algal associations are predicted to be lower at both ends of the light intensity gradient due to reduced resource heterogeneity and stronger competition7. Moreover, the reduced translocation of photosynthetic usable energy can lead to increased risk of species extinction and prevalence of few efficient competitors at exploiting the available light energy, either in excess or deficit.
Given their mixotrophic nature, heterotrophy is another aspect that has to be considered when analyzing the energy budget of zooxanthellate corals and its potential influence on biodiversity patterns across depths. Previous studies have demonstrated that some coral species are able to increase their metabolic reliance on heterotrophy to compensate for reduced photosynthetically derived energy acquisition in deep, low-light environments58–60, thereby potentially influencing biodiversity patterns across depths. Although we did not parameterize this aspect of the symbiosis in the documented productivity-biodiversity model, a potential effect of heterotrophic plasticity or trophic niche differentiation on coral richness cannot be discharged. However, the large component of the variability explained by the model and the contrasting features exhibited by zooxanthellate (non-facultative) corals suggest that coral adaptation and specialization to optimize solar energy utilization may have been a key driving force in coral evolution, more than enhancing heterotrophic feeding capabilities41,50. For instance, if heterotrophy plays a significant role in determining patterns of coral biodiversity with depth, a greater number of species with morphologies that facilitate suspension feeding (e.g., branching) will be expected to thrive with increasing depth. However, the empirical evidence indicates that flattened morphologies to maximize light capture prevail in the lower photic zone41,50.
Disturbance frequency and intensity have also been shown to affect the structure of coral communities, and it has been traditionally hypothesized that intermediate disturbance regimes lead to greater biodiversity20. The intermediate disturbance hypothesis, originally proposed as a conceptual model, has been supported and rejected in its capacity for explaining biodiversity patterns in ecological communities, both aquatic and terrestrial (reviewed in Rosenzweig and Abramsky7, and Huston10). There are two major disturbances that can frequently affect shallow-water reefs, with little impact in deep-water counterparts: coral bleaching related to heat stress and high wave energy due to storms and hurricanes18,41. These disturbances can certainly influence both the local species diversity and the community composition of symbiotic corals21,22. However, the consistency of the explanatory power of the productivity-biodiversity model despite local environmental and ecological conditions among sites suggests that disturbances and other environmental factors may alter the location of the node as well as the slope of the increasing and/or decreasing phase of the unimodal curve, but not the overall pattern. Indeed, our results suggest that ignoring the role of productivity can obscure the underlying cause of biodiversity patterns in coral communities.
In summary, the results of this analysis indicate that solar energy and photosynthetic productivity are major driving forces of biodiversity patterns along depth gradients in symbiotic coral communities. The symbiosis with photosynthesizing dinoflagellates was a successful adaptive solution for corals to thrive in oligotrophic environments 13 which, ultimately, led to the consolidation of one of the most biodiverse ecosystems on the planet. The gradient of downwelling irradiance mediated by the water optical properties coupled with the metabolic and physiological constraints imposed by the photosymbiosis seems to be primary determinants for the establishment of global-scale patterns of biodiversity in scleractinian corals and, potentially, associated communities that depend on them for food and shelter. The increased environmental degradation of the water optical quality associated with coastal development, nutrient enrichment, massive algal blooms, and terrestrial runoff to which most of the world’s reefs are currently exposed61–64, may be an important underlying cause of biodiversity erosion and change in the assemblage structure of coral reef communities. Local conservation actions seeking to maintain the water optical quality and the underwater light climate are essential to preserve coral biodiversity, while concerted global action to limit greenhouse emissions and slow global warming continues to move forward.