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      Effects of surface geometry on light exposure, photoacclimation and photosynthetic energy acquisition in zooxanthellate corals

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          Abstract

          Symbiotic corals display a great array of morphologies, each of which has unique effects on light interception and the photosynthetic performance of in hospite zooxanthellae. Changes in light availability elicit photoacclimation responses to optimize the energy balances in primary producers, extensively documented for corals exposed to contrasting light regimes along depth gradients. Yet, response variation driven by coral colony geometry and its energetic implications on colonies with contrasting morphologies remain largely unknown. In this study, we assessed the effect of the inclination angle of coral surface on light availability, short- and long-term photoacclimation responses, and potential photosynthetic usable energy. Increasing surface inclination angle resulted in an order of magnitude reduction of light availability, following a linear relationship explained by the cosine law and relative changes in the direct and diffuse components of irradiance. The light gradient induced by surface geometry triggered photoacclimation responses comparable to those observed along depth gradients: changes in the quantum yield of photosystem II, photosynthetic parameters, and optical properties and pigmentation of the coral tissue. Differences in light availability and photoacclimation driven by surface inclination led to contrasting energetic performance. Horizontally and vertically oriented coral surfaces experienced the largest reductions in photosynthetic usable energy as a result of excessive irradiance and light-limiting conditions, respectively. This pattern is predicted to change with depth or local water optical properties. Our study concludes that colony geometry plays an essential role in shaping the energy balance and determining the light niche of zooxanthellate corals.

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          Heterotrophy in tropical scleractinian corals.

          The dual character of corals, that they are both auto- and heterotrophs, was recognized early in the twentieth Century. It is generally accepted that the symbiotic association between corals and their endosymbiotic algae (called zooxanthellae) is fundamental to the development of coral reefs in oligotrophic tropical oceans because zooxanthellae transfer the major part of their photosynthates to the coral host (autotrophic nutrition). However, numerous studies have confirmed that many species of corals are also active heterotrophs, ingesting organisms ranging from bacteria to mesozooplankton. Heterotrophy accounts for between 0 and 66% of the fixed carbon incorporated into coral skeletons and can meet from 15 to 35% of daily metabolic requirements in healthy corals and up to 100% in bleached corals. Apart from this carbon input, feeding is likely to be important to most scleractinian corals, since nitrogen, phosphorus, and other nutrients that cannot be supplied from photosynthesis by the coral's symbiotic algae must come from zooplankton capture, particulate matter or dissolved compounds. A recent study showed that during bleaching events some coral species, by increasing their feeding rates, are able to maintain and restore energy reserves. This review assesses the importance and effects of heterotrophy in tropical scleractinian corals. We first provide background information on the different food sources (from dissolved organic matter to meso- and macrozooplankton). We then consider the nutritional inputs of feeding. Finally, we review feeding effects on the different physiological parameters of corals (tissue composition, photosynthesis and skeletal growth).
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            Photoprotection in plants: a new light on photosystem II damage.

            Sunlight damages photosynthetic machinery, primarily photosystem II (PSII), and causes photoinhibition that can limit plant photosynthetic activity, growth and productivity. The extent of photoinhibition is associated with a balance between the rate of photodamage and its repair. Recent studies have shown that light absorption by the manganese cluster in the oxygen-evolving complex of PSII causes primary photodamage, whereas excess light absorbed by light-harvesting complexes acts to cause inhibition of the PSII repair process chiefly through the generation of reactive oxygen species. As we review here, PSII photodamage and the inhibition of repair are therefore alleviated by photoprotection mechanisms associated with avoiding light absorption by the manganese cluster and successfully consuming or dissipating the light energy absorbed by photosynthetic pigments, respectively. Copyright © 2010 Elsevier Ltd. All rights reserved.
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              Energy balance and acclimation to light and cold

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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Funding acquisitionRole: InvestigationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS One
                plos
                PLOS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                3 January 2024
                2024
                : 19
                : 1
                : e0295283
                Affiliations
                [1 ] Department of Biology, The Pennsylvania State University, University Park, Pennsylvania, United States of America
                [2 ] Unidad Académica Puerto Morelos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Cancún, México
                University of Bologna, ITALY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0001-9486-7809
                Article
                PONE-D-23-21541
                10.1371/journal.pone.0295283
                10763928
                38ec8011-72fa-47a9-94b4-2212cbce13da
                © 2024 López-Londoño et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 10 July 2023
                : 17 November 2023
                Page count
                Figures: 6, Tables: 0, Pages: 21
                Funding
                Funded by: Consejo Nacional de Ciencia y Tecnología de México
                Award Recipient :
                Funded by: Consejo Nacional de Ciencia y Tecnología de México
                Award ID: Project 129880, Conv-CB-2009
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100006087, Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México;
                Award Recipient :
                TLL was supported by a scholarship from the Consejo Nacional de Ciencia y Tecnología (CONACYT) from México and by Pennsylvania State University startup funds to RIP. Research funding for SE and RIP was provided by CONACYT-Mexico (Project 129880, Conv-CB-2009). A PASPA fellowship from the DGAPA-UNAM supported the visit of SE to the Biology Department at Pennsylvania State University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. There was no additional external funding received for this study.
                Categories
                Research Article
                Biology and Life Sciences
                Marine Biology
                Corals
                Earth Sciences
                Marine and Aquatic Sciences
                Marine Biology
                Corals
                Physical Sciences
                Physics
                Electromagnetic Radiation
                Light
                Biology and Life Sciences
                Biochemistry
                Plant Biochemistry
                Photosynthesis
                Biology and Life Sciences
                Plant Science
                Plant Biochemistry
                Photosynthesis
                Biology and Life Sciences
                Marine Biology
                Coral Reefs
                Earth Sciences
                Marine and Aquatic Sciences
                Marine Biology
                Coral Reefs
                Earth Sciences
                Marine and Aquatic Sciences
                Reefs
                Coral Reefs
                Biology and Life Sciences
                Species Interactions
                Symbiosis
                Physical Sciences
                Chemistry
                Physical Chemistry
                Photochemistry
                Biology and Life Sciences
                Ecology
                Ecological Metrics
                Photosynthetic Efficiency
                Ecology and Environmental Sciences
                Ecology
                Ecological Metrics
                Photosynthetic Efficiency
                Biology and Life Sciences
                Biochemistry
                Plant Biochemistry
                Photosynthesis
                Photosynthetic Efficiency
                Biology and Life Sciences
                Plant Science
                Plant Biochemistry
                Photosynthesis
                Photosynthetic Efficiency
                Physical Sciences
                Physics
                Electromagnetic Radiation
                Light
                Sunlight
                Physical Sciences
                Physics
                Electromagnetic Radiation
                Solar Radiation
                Sunlight
                Custom metadata
                All relevant data are within the paper and its Supporting Information files. Additionally, the data relevant to this study are available from figshare at https://doi.org/10.6084/m9.figshare.24599499.v1.

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