Photosynthetic usable energy explains vertical patterns of biodiversity in zooxanthellate corals

doi:10.21203/rs.3.rs-1746204/v1

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Photosynthetic usable energy explains vertical patterns of biodiversity in zooxanthellate corals

https://doi.org/10.21203/rs.3.rs-1746204/v1

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The biodiversity in coral reef ecosystems is distributed heterogeneously across spatial and temporal scales, being commonly influenced by biogeographic factors, habitat area and disturbance frequency. In contrast to terrestrial environments, a potential association between gradients of usable energy and biodiversity has received little empirical support for explaining such patterns. Here, we analyzed the productivity and biodiversity variation over depth gradients in symbiotic coral communities, whose members rely on the energy translocated by photosynthetic algal symbionts (zooxanthellae). A mechanistic model was used to simulate the depth-dependent variation in photosynthetic usable energy to corals and explore its relationship with gradients of species diversity, comparing reefs with contrasting water clarity and biodiversity patterns along global hotspots of marine biodiversity. The productivity-biodiversity model explained between 64% and 95% of the depth-related variation in coral species richness, indicating that much of the variation in coral biodiversity with depth is driven by changes in the fractional contribution of photosynthetically fixed energy by the zooxanthellae. These results suggest a fundamental role of solar energy availability and photosynthetic productivity on global-scale patterns of coral biodiversity and community structure across depths. Accordingly, the maintenance of water optical quality is fundamental to protect coral biodiversity and prevent reef degradation, in addition to climate change mitigation policies.

Sunlight is the major source of energy for virtually the entire biochemical production of organic matter on Earth¹. Among the different factors affecting primary producers both in terrestrial and aquatic ecosystems, sunlight is perhaps the most spatially and temporally heterogeneous, resulting in significant impacts on the energy transfer across trophic levels^2–4. The variation in the supply of usable energy derived from primary production plays an important role on the spatial variation of species diversity in ecological communities, facilitating a decreased risk of species extinction from demographic and environmental stochasticity in highly productive environments⁵. Although a positive productivity-biodiversity relationship prevails in terrestrial and aquatic ecosystems⁶, significant debate remains over the strength of the linkage between these two features and whether it is predictable, considering the observed variations in the form of productivity-biodiversity relationship in some communities (e.g., positive, negative, unimodal and neutral)^7–12. Since the amount of usable energy by a group of organisms in a community is difficult to measure directly, part of this variation has been associated with the surrogates used as roughly indicative of productivity and the confounding effects of environmental stressors, typically more accentuated in highly productive environments^6,7.

Scleractinian corals are calcified metazoans responsible for building the most diverse and productive marine ecosystem from which humans obtain essential socio-economic benefits. The ecological and evolutionary success of these animals in oligotrophic environments since the Late Triassic is attributed to the nutritional endosymbiosis with photosynthetic unicellular algae (zooxanthellae)¹³, which confers on them the capacity to use sunlight as the major source of energy increasing their rates of calcification^14,15. Due to the exponential attenuation of sunlight with depth¹⁶, the vertical distribution of symbiotic corals occurs along steep gradients governed by light in small spatial scales, while other limiting resources and physical factors (e.g., nitrogen, oxygen, temperature) vary less or remain nearly constant^17,18. Corals are also exposed to significant changes in light intensity in response to the optical properties of the water column (i.e., vertical attenuation coefficient for downwelling irradiance, K_d), as benthic, sessile organisms prevalent in coastal waters. This variation is determined by precipitation patterns and seaward fluxes of terrestrial nutrients and sediments^16,19, having important implications on the primary production and energy balance of coral communities^3,4. However, a relationship between gradients of productivity and biodiversity in coral communities has not yet been demonstrated, and patterns of coral biodiversity are primarily attributed to biogeographic factors, habitat area and disturbance frequency^12,20−26.

The obligatory nature of the endosymbiosis between a primary producer and an animal, together with the distribution of corals along strong gradients of sunlight energy with depth, make coral communities particularly interesting for exploring the relationship between primary productivity and consumer-species diversity. Using a mechanistic model based on underwater optics and physiological principles, we estimated the variation in photosynthetic usable energy supplied by the symbiotic algae to coral hosts and examined its association with patterns of coral species diversity across depth gradients. We further tested the model using published datasets from reefs with contrasting evolutionary histories, environmental conditions, and patterns of coral species diversity, encompassing the three major hotspots of global marine biodiversity. Our analysis shows that much of the variation in coral diversity with depth is explained by changes in photosynthetic usable energy, providing strong support to a mechanistic link between productivity and biodiversity in coral communities.

Zooxanthellae’ energy budget is variable and nonlinearly related to light availability

The diurnal patterns of change of the photosystem II (PSII) effective quantum yield (ΔF/F_m’) measured with pulse amplitude modulated (PAM) fluorometry, followed the well-known inverse relationship with light availability, as it decreases after dawn to reach minimum values at midday and then gradually recovers by dusk^{27 − 29}. However, the maximum reduction of ΔF/F_m’ at noon and its recovery by late afternoon are not consistent between days, showing an incomplete recovery when the light exposure increases and full recovery exceeding former dawn levels when the light exposure is reduced (Fig. 1a). The relationship between PSII half-time (t_1/2) and light exposure is non-linear and can be described using a power-function model (R² = 0.97, p < 0.01) (Fig. 1b). Similar patterns have been observed in other primary producers^30,31, including several species of reef-building corals (Gómez-Campo Ph.D. thesis, unpublished data), suggesting that the non-linearity between PSII t_1/2 and available irradiance may be driven by common mechanisms across coral species. A conceptual analysis of the changes in the maximum excitation pressure over PSII (Q_m) as a function of irradiance indicates that both the shortage as well as the excess of light compromise the energetic performance of coral holobionts (Fig. 1c). This compromise results from two contrasting effects: a negligible photosynthetic activity of the zooxanthellae under light-limiting conditions (low Q_m), and increased costs of repair from photodamage under excessive irradiance due to full saturation of the photosynthetic apparatus (high Q_m)^32,33.

The non-linearity between downwelling irradiance, photosynthetic production and energy expenditure in photorepair, leads to a unimodal, hump-shaped pattern of the photosynthetic usable energy to corals with depth (Fig. 1d). This pattern is associated with an energetic imbalance that results from the hyperbolic response of photosynthesis to light (i.e., saturation above the light saturation point, E_k), and the linear relationship between light availability and light absorption^34–36. The decline in usable energy toward both ends of the depth gradient is explained by two different processes: 1) in shallow high-light environments, the energy expenditure in photorepair increases proportionally to the available irradiance while photosynthesis remains constant; and 2) in deep low-light environments, the light attenuation results in a gradual decline of the photosynthetic carbon fixation. At a particular intermediate depth, where the absorbed irradiance is close to that required for maximizing photosynthesis (≈E_k), the supply of photosynthetic usable energy and the holobiont energetic performance are predicted to reach maximum potential.

Photosynthetic usable energy correlates with coral biodiversity patterns

The coral productivity-biodiversity model explained most of the variation in coral species number with depth in all reefs tested (Fig. 2, Supplementary Tables 1, 2). The explanatory power of the model was consistently high, between 80% and 95%, in sites with unimodal relationships between species richness and depth (e.g., atolls from the Chagos Archipelago in the Indian Ocean³⁷, Discovery Bay in the Caribbean³⁸, and Kimbe Bay in the Indo-Pacific¹²). The model also captured the overall pattern of change in species number with depth in sites with monotonic patterns, both positive (Gulf of Eilat, Red Sea³⁹) and negative (Pulau Hantu, Singapore⁴⁰). In these sites, the model respectively explained 64% and 75% of species number variation, and in the site with a positive, monotonic relationship, it predicted a reduction in species number toward non-sampled depths below ~ 40 m, suggesting that these monotonic patterns may represent only one-half of the unimodal productivity-biodiversity relationship depending on whether the sampled depth range was located above or below the mode (Fig. 2).

The K_d’s in sites with unimodal relationships were consistently low (between 0.06 m^− 1 and 0.082 m^− 1)^12,38,41. In contrast, in sites with positive and negative monotonic relationships, the K_d’s were respectively the lowest and highest of all sites considered in our analysis (0.047 m^− 1 and 0.303 m^− 1)^40,41 (Supplementary Table 2). The deepest record of maximum coral species richness by location was associated with the water optical quality and light propagation into the water column, determined by the K_d. A non-linear association between both parameters was observed and described using a power function (R² = 0.98, p < 0.01, Fig. 3a), indicating a fast reduction in the depth of maximum coral richness with increasing K_d (Fig. 3a). The overall change in coral diversity along a common light intensity gradient normalized to the percentage of surface irradiance, followed a unimodal, bell-shaped pattern with an overall reduction in the relative number of species at both ends of the light gradient mediated by the local K_d (Fig. 3b).

The pattern of change of the photosystem II (PSII) effective quantum yield (ΔF/F_m’) 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 energy^{27 − 29}. Differences in ΔF/F_m’ 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 (t_1/2) 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 producers^42,43.

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 environments^5,6,23. 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 studied^5–7.

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 K_d). 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 K_d 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 conditions^3,46, and that a single K_d 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 production^4,19, is beyond the scope of this study.

Zooxanthellate corals display contrasting photoacclimation responses, coral cover, colony morphologies and genetic richness along depth gradients^32,47−53, 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 habitats^47,53. 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 capture^48–51. 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 colonies^32,54−57. 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 environments^58–60, 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 capabilities^41,50. 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 zone^41,50.

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 hurricanes^18,41. These disturbances can certainly influence both the local species diversity and the community composition of symbiotic corals^21,22. 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 exposed^61–64, 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.

Zooxanthellae’ energy budget

We assume that the energy cost of repairing the light-induced damage of the photosynthetic apparatus in zooxanthellae is the main limiting factor for the photosynthetic usable energy supply by the zooxanthellae to corals. 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 producers^42,43. The photosynthetic usable energy supply to corals is correlative to the “contribution of zooxanthellae carbon to the animal host respiration”, a concept originally introduced by Muscatine et al.⁶⁵. In their original formulation, however, the translocation of photosynthetically fixed carbon was calculated based on the oxygen production/consumption of the holobiont using a factor that was independent of light availability.

We determined the pattern of change of the zooxanthellae energy expenditure in photorepair as a function of light exposure using small fragments (~ 5x5 cm, n = 50) of the Caribbean coral Porites astreoides collected from La Bocana Reef at 5 m depth in Puerto Morelos, México. Two weeks after acclimation in a running seawater aquarium with neutral density filters simulating the light intensity at the collection depth and controlling temperature at 28 °C, corals were exposed to contrasting light intensities to measure changes in: 1) the photosystem II (PSII) photochemical quantum yield (ΔF/F_m’) over diurnal cycles using pulse amplitude modulated technique³², and 2) the PSII half-time (t_1/2) by analyzing the diurnal oscillations of ΔF/F_m’ of coral fragments exposed to 100 µg of chloramphenicol (CAP), a chloroplast protein-synthesis inhibitor⁶⁶.

The PSII t_1/2 was calculated as the amount of time required to inactivate 50% of the PSII. We explored the optimum relationship between PSII t_1/2 and light exposure (% of sea surface) using power-function modeling. The following power function explained the relationship of the PSII t_1/2 to the available irradiance along the depth gradient:

PSII t_1/2 = M E_z ^Δ, (Eq. 1)

where M is the maximum PSII t_1/2 when the available irradiance tends to 0, E_z is irradiance at depth z relative to incident irradiance at sea surface, and Δ is the rate of change of PSII t_1/2 with respect to available irradiance.

The energy expenditure in photorepair by the zooxanthellae over a diurnal cycle (C_z) was calculated through the relation:

C _z = (12 / PSII t_1/2) R, (Eq. 2)

where R corresponds to the relative energy cost of protein turnover for the reassembly of PSII reaction centers over a diurnal cycle (12 h of daylight).

Description of the coral productivity-biodiversity model

To analyze the relationship between photosynthetic usable energy and coral biodiversity across depths, we used a numerical model with a lumped-parameter approach assuming that a specific set of parameters represent the average response of the whole community⁶⁷. The model acknowledged three physical and physiological principles that govern the vertical distribution of light in the water column and the photosynthetic activity of primary producers: 1) solar radiation diminishes exponentially with depth according to the water optical properties (i.e., local K_d); 2) algal photosynthetic production describes a hyperbolic tangent response to light availability; and 3) energy expenditure for maintaining the algal photosynthetic activity is mediated by the light exposure following Eq. 2. This approach allows us to draw general conclusions about light-driven processes at the community level at the expense of simplifying the complex dynamics of the water optical properties^3,19,46, and acclimation strategies of corals to maximize performance under particular light and temperature regimes^49,68,69.

The available solar radiation across depths, as the energy source for the symbiotic algae to fix inorganic carbon via photosynthesis, is calculated following Kirk¹⁶ as:

E _z = E₀ e^{− Kd z} (Eq. 3),

where E_z and E₀ are the irradiance (E) at depth z and just below the sea surface, respectively.

The hyperbolic response of algal photosynthesis (P_g) to irradiance is calculated according to Jassby and Platt³⁴, as:

P _g = P_max tanh (α E_z / P_max) (Eq. 4),

where α is the photosynthetic efficiency corresponding to the slope of the linear increase of photosynthesis at subsaturating irradiance and P_max is the maximum photosynthetic rates at light saturation. We assume no temporal reduction in light-saturated photosynthesis in response to photoinhibition at excessive irradiance considering the apparent absence of this phenomenon in symbiotic dinoflagellates in hospite²⁸.

Finally, the photosynthetic usable energy supply (PUES) is parameterized with the following equation:

PUES = P_g - C_s (Eq. 5).

Testing the coral productivity-biodiversity model

We tested the explanatory power of the productivity-biodiversity model in a wide range of coral reef habitats along the world’s major hotspots of marine biodiversity (Indo-Pacific, Caribbean and Indian Ocean^70,71). We analyzed published datasets from studies that reported the change in number of symbiotic coral species with depth in seven reefs with contrasting geological history, environmental conditions and biodiversity patterns (unimodal, monotonic increase and monotonic decrease) (Supplementary Table 1)^12,37−40. Data were extracted directly from the text, tables, or original datasets. When the data was only presented in graphical format, raw values were extracted using the software WebPlotDigitizer version 4.4 (https://automeris.io/WebPlotDigitizer). When the local K_d was not reported in the manuscript, it was calculated from the light change across depths following Eq. 3. When neither of these options was available, it was extracted from the literature for the same or comparable sites (Supplementary Table 2).

For each site, a two-step optimization procedure was used to calculate those parameters that could not be estimated independently with empirical data (M, Δ, P_max, α, R) (Supplementary Table 2). The optimization of these parameters produced the best possible fit between the model output and the mean number of observed species across depths. First, an iterative algorithm that allows the variation of each parameter within a suspected range while fulfilling the model equations exactly was used for fitting a linear model with coral richness as a function of the photosynthetic usable energy. Using the Akaike Information Criterion (AIC), we selected the set of values that minimized the misfit between the productivity-biodiversity model output and the empirical data. Then, the values of the targeted parameters that minimized the AIC were used as the starting values in a bound-constrained minimization algorithm (optim function) based on the Nelder-Mead method⁷². The lower and upper bounds of each parameter were determined based on empiric data and physiological limits and were constant among sites. A diurnal cycle of solar radiation describing a 12h sinusoidal curve peaking at 1,800 µmol quanta m^− 2 s^− 1 at noon was used as forcing function (chosen maximum is a random value close to naturally occurring maximum irradiance at ocean surface in tropical areas ¹⁶). All analyses were conducted using R version 3.6.1⁷³.

Acknowledgments

We dedicate this manuscript to the memory of Professor Robert (Bob) K. Trench, a seminal figure for our current understanding of algal invertebrate symbioses. The authors thank Todd LaJeunesse, Mitzy F. Porras, Carlos Prada, Teresa Morán-López and M. Isabel Martínez-Rugerio for their valuable contributions; the National Commission on Aquaculture and Fisheries (CONAPESCA) for research permit (DGOPA 08606.251011.3021). This work was supported by Pennsylvania State University startup funds to RI-P.

Author contributions

TL-L, KG-C, SE and RI-P designed the study. XH-P and KG-C conducted coral experiments. TL-L conducted meta-analysis and eco-physiological modelling under the supervision of SE and RI-P. TL-L and RI-P wrote the manuscript with contributions and feedback from all authors. All authors read and approved the final version of the manuscript.

Competing interests

The authors declare no competing interests.

Data and code availability

Data generated and analyzed during the current study, as well as the code used to run these analyses, are openly available on Figshare (https://figshare.com/s/b73708c98e8108ec0352).

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No competing interests reported.

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Photosynthetic usable energy explains vertical patterns of biodiversity in zooxanthellate corals

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Abstract

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Introduction

Results

Zooxanthellae’ energy budget is variable and nonlinearly related to light availability

Photosynthetic usable energy correlates with coral biodiversity patterns

Discussion

Methods

Zooxanthellae’ energy budget

Description of the coral productivity-biodiversity model

Testing the coral productivity-biodiversity model

Declarations

References

Additional Declarations

Supplementary Files

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Version 1