Light quantity and quality are among the most important factors determining the physiology and stress response of zooxanthellate corals. Yet, almost nothing is known about the light field that Symbiodinium experiences within their coral host, and the basic optical properties of coral tissue are unknown. We used scalar irradiance microprobes to characterize vertical and lateral light gradients within and across tissues of several coral species. Our results revealed the presence of steep light gradients with photosynthetically available radiation decreasing by about one order of magnitude from the tissue surface to the coral skeleton. Surface scalar irradiance was consistently higher over polyp tissue than over coenosarc tissue in faviid corals. Coral bleaching increased surface scalar irradiance by ~150% (between 500 and 700 nm) relative to a healthy coral. Photosynthesis peaked around 300 μm within the tissue, which corresponded to a zone exhibiting strongest depletion of scalar irradiance. Deeper coral tissue layers, e.g., ~1000 μm into aboral polyp tissues, harbor optical microniches, where only ~10% of the incident irradiance remains. We conclude that the optical microenvironment of corals exhibits strong lateral and vertical gradients of scalar irradiance, which are affected by both tissue and skeleton optical properties. Our results imply that zooxanthellae populations inhabit a strongly heterogeneous light environment and highlight the presence of different optical microniches in corals; an important finding for understanding the photobiology, stress response, as well as the phenotypic and genotypic plasticity of coral symbionts.
Coral tissue optics has received very little attention in the past, although the interaction between tissue and light is central to our basic understanding of coral physiology. Here we used fibre-optic and electrochemical microsensors along with variable chlorophyll fluorescence imaging to directly measure lateral light propagation within living coral tissues. Our results show that corals can transfer light laterally within their tissues to a distance of ~2 cm. Such light transport stimulates O 2 evolution and photosystem II operating efficiency in areas >0.5-1 cm away from direct illumination. Light is scattered strongly in both coral tissue and skeleton, leading to photon trapping and lateral redistribution within the tissue. Lateral light transfer in coral tissue is a new mechanism by which light is redistributed over the coral colony and we argue that tissue optical properties are one of the key factors in explaining the high photosynthetic efficiency of corals.
The light field on coral reefs varies in intensity and spectral composition, and is the key regulating factor for phototrophic reef organisms, for example scleractinian corals harbouring microalgal symbionts. However, the actual efficiency of light utilization in corals and the mechanisms affecting the radiative energy budget of corals are underexplored. We present the first balanced light energy budget for a symbiont-bearing coral based on a fine-scale study of the microenvironmental photobiology of the massive coral Montastrea curta. The majority (more than 96%) of the absorbed light energy was dissipated as heat, whereas the proportion of the absorbed light energy used in photosynthesis was approximately 4.0% under an irradiance of 640 mmol photons m 22 s 21. With increasing irradiance, the proportion of heat dissipation increased at the expense of photosynthesis. Despite such low energy efficiency, we found a high photosynthetic efficiency of the microalgal symbionts showing high gross photosynthesis rates and quantum efficiencies (QEs) of approximately 0.1 O 2 photon 21 approaching theoretical limits under moderate irradiance levels. Corals thus appear as highly efficient light collectors with optical properties enabling light distribution over the corallite/tissue microstructural canopy that enables a high photosynthetic QE of their photosynthetic microalgae in hospite.
We used a novel diver-operated microsensor system to collect in situ spectrally resolved light fields on corals with a micrometer spatial resolution. The light microenvironment differed between polyp and coenosarc tissues with scalar irradiance (400-700 nm) over polyp tissue, attenuating between 5.1-and 7.8-fold from top to base of small hemispherical coral colonies, whereas attenuation was at most 1.5-fold for coenosarc tissue. Fluctuations in ambient solar irradiance induced changes in light and oxygen microenvironments, which were more pronounced and faster in coenosarc compared with polyp tissue. Backscattered light from the surrounding benthos contributed . 20% of total scalar irradiance at the coral tissue surface and enhanced symbiont photosynthesis and the local O 2 concentration, indicating an important role of benthos optics for coral ecophysiology. Light fields on corals are species and tissue specific and exhibit pronounced variation on scales from micrometers to decimeters. Consequently, the distribution, genetic diversity, and physiology of coral symbionts must be coupled with the measurements of their actual light microenvironment to achieve a more comprehensive understanding of coral ecophysiology.
Green fluorescent protein (GFP)-like pigments have been proposed to have beneficial effects on coral photobiology. Here, we investigated the relationships between green fluorescence, coral heating and tissue optics for the massive coral Dipsastraea sp. (previously Favia sp.). We used microsensors to measure tissue scalar irradiance and temperature along with hyperspectral imaging and combined imaging of variable chlorophyll fluorescence and green fluorescence. Green fluorescence correlated positively with coral heating and scalar irradiance enhancement at the tissue surface. Coral tissue heating saturated for maximal levels of green fluorescence. The action spectrum of coral surface heating revealed that heating was highest under red (peaking at 680 nm) irradiance. Scalar irradiance enhancement in coral tissue was highest when illuminated with blue light, but up to 62% (for the case of highest green fluorescence) of this photon enhancement was due to green fluorescence emission. We suggest that GFP-like pigments scatter the incident radiation, which enhances light absorption and heating of the coral. However, heating saturates, because intense light scattering reduces the vertical penetration depth through the tissue eventually leading to reduced light absorption at high fluorescent pigment density. We conclude that fluorescent pigments can have a central role in modulating coral light absorption and heating.
Corals are very efficient at using solar radiation, with photosynthetic quantum efficiencies approaching theoretical limits. Here, we investigated potential mechanisms underlying such outstanding photosynthetic performance through extracting inherent optical properties of the living coral tissue and skeleton in a massive faviid coral. Using Monte Carlo simulations developed for medical tissue optics it is shown that for the investigated faviid coral, the coral tissue was a strongly light scattering matrix with a reduced scattering coefficient of μs’ = 10 cm-1 (at 636 nm). In contrast, the scattering coefficient of the coral skeleton was μs’ = 3.4 cm-1, which facilitated the efficient propagation of light to otherwise shaded coral tissue layers, thus supporting photosynthesis in lower tissues. Our study provides a quantification of coral tissue optical properties in a massive faviid coral and suggests a novel light harvesting strategy, where tissue and skeletal optics act in concert to optimize the illumination of the photosynthesizing algal symbionts embedded within the living coral tissue.
Climate change-related coral bleaching, i.e., the visible loss of zooxanthellae from the coral host, is increasing in frequency and extent and presents a major threat to coral reefs globally. Coral bleaching has been proposed to involve accelerating light stress of their microalgal endosymbionts via a positive feedback loop of photodamage, symbiont expulsion and excess in vivo light exposure. To test this hypothesis, we used light and O2 microsensors to characterize in vivo light exposure and photosynthesis of Symbiodinium during a thermal stress experiment. We created tissue areas with different densities of Symbiodinium cells in order to understand the optical properties and light microenvironment of corals during bleaching. Our results showed that in bleached Pocillopora damicornis corals, Symbiodinium light exposure was up to fivefold enhanced relative to healthy corals, and the relationship between symbiont loss and light enhancement was well-described by a power-law function. Cell-specific rates of Symbiodinium gross photosynthesis and light respiration were enhanced in bleached P. damicornis compared to healthy corals, while areal rates of net photosynthesis decreased. Symbiodinium light exposure in Favites sp. revealed the presence of low light microniches in bleached coral tissues, suggesting that light scattering in thick coral tissues can enable photoprotection of cryptic symbionts. Our study provides evidence for the acceleration of in vivo light exposure during coral bleaching but this optical feedback mechanism differs between coral hosts. Enhanced photosynthesis in relation to accelerating light exposure shows that coral microscale optics exerts a key role on coral photophysiology and the subsequent degree of radiative stress during coral bleaching.
BackgroundCoral reefs degrade globally at an alarming rate, with benthic algae often replacing corals. However, the extent to which benthic algae contribute to coral mortality, and the potential mechanisms involved, remain disputed. Recent laboratory studies suggested that algae kill corals by inducing hypoxia on the coral surface, through stimulated microbial respiration.Methods/FindingsWe examined the main premise of this hypothesis by measuring in situ oxygen microenvironments at the contact interface between the massive coral Porites spp. and turf algae, and between Porites spp. and crustose coralline algae (CCA). Oxygen levels at the interface were similar to healthy coral tissue and ranged between 300–400 µM during the day. At night, the interface was hypoxic (∼70 µM) in coral-turf interactions and close to anoxic (∼2 µM) in coral-CCA interactions, but these values were not significantly different from healthy tissue. The diffusive boundary layer (DBL) was about three times thicker at the interface than above healthy tissue, due to a depression in the local topography. A numerical model, developed to analyze the oxygen profiles above the irregular interface, revealed strongly reduced net photosynthesis and dark respiration rates at the coral-algal interface compared to unaffected tissue during the day and at night, respectively.Conclusions/SignificanceOur results showed that hypoxia was not a consistent feature in the microenvironment of the coral-algal interface under in situ conditions. Therefore, hypoxia alone is unlikely to be the cause of coral mortality. Due to the modified topography, the interaction zone is distinguished by a thicker diffusive boundary layer, which limits the local metabolic activity and likely promotes accumulation of potentially harmful metabolic products (e.g., allelochemicals and protons). Our study highlights the importance of mass transfer phenomena and the need for direct in situ measurements of microenvironmental conditions in studies on coral stress.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.