Photosynthesis and Bio-Optical Properties of Fluorescent Mesophotic Corals

Mesophotic coral ecosystems (MCEs) are light-dependent coral-associated communities found at 30–150 m depth. Corals inhabiting these deeper reefs are often acclimatized to a limited and blue-shifted light environment, enabling them to maintain the relationship with their photosynthetic algal symbionts (family Symbiodiniaceae) despite the seemingly suboptimal light conditions. Among others, fluorescent proteins produced by the coral host may play a role in the modulation of the quality and spectral distribution of irradiance within the coral tissue through wavelength transformation. Here we examined the bio-optical properties and photosynthetic performances of different fluorescence morphs of two mesophotic coral species Goniopora minor and Alveopora ocellata, in order to test the photosynthesis enhancement hypothesis proposed for coral fluorescence. The green morph of G. minor and the low fluorescence morph of A. ocellata exhibit, in their natural habitats, higher abundance. The morphs also presented different spectral reflectance and light attenuation within the tissue. Nevertheless, chlorophyll a fluorescence-based, and O2 evolution measurements, revealed only minor differences between the photosynthetic abilities of three fluorescence morphs of the coral G. minor and two fluorescence morphs of A. ocellata. The fluorescence morphs did not differ in their algal densities or chlorophyll concentrations and all corals harbored Symbiodiniaceae from the genus Cladocopium. Thus, despite the change in the internal light quantity and quality that corals and their symbionts experience, we found no evidence for the facilitation or enhancement of photosynthesis by wavelength transformation.</jats:p

Energy allocation trade-offs as a function of age in fungiid corals

To compete effectively, living organisms must adjust the allocation of available energy resources for growth, survival, maintenance, and reproduction throughout their life histories. Energy demands and allocations change throughout the life history of an organism, and understanding their energy allocation strategies requires determination of the relative age of individuals. As most scleractinian corals are colonial, the relationship between age and mass/size is complicated by colony fragmentation, partial mortality, and asexual reproduction. To overcome these limitations, solitary mushroom corals, Herpolitha limax from Okinawa, Japan and Fungia fungites from Okinawa and the Great Barrier Reef (GBR), Australia, were used to investigate how energy allocation between these fundamental processes varies as a function of age. Measurements of the relative growth, biochemical profiles, fecundity of individuals of different sizes, and the settlement success of their progeny have revealed physiological trade-offs between growth and reproduction, with increasing body mass ultimately leading to senescence. The importance of energy allocation for reproduction led us to examine the reproductive strategies and sex allocation in the two studied species. In the present study, the smallest individuals of both species studied were found to invest most of their energy in relative growth, showing higher lipid and carbohydrate content than the later stages. In medium-sized corals, this pattern was overturned in favour of reproduction, manifesting in terms of both the highest fecundity and settlement success of the resulting brooded larvae. Finally, a phase of apparent senescence was observed in the largest individuals, characterized by a decrease in most of the parameters measured. In addition, complex reproductive plasticity has been revealed in F. fungites in the GBR, with individual females releasing eggs, embryos, planulae, or a combination of these. These data provide the most direct estimates currently available for physiological, age-related trade-offs during the life history of a coral. The unusual reproductive characteristics of the GBR F. fungites indicate previously unknown layers of complexity in the reproductive biology of corals and have implications for their adaptive potential across a wide geographical scale

Spectral Diversity and Regulation of Coral Fluorescence in a Mesophotic Reef Habitat in the Red Sea

The phenomenon of coral fluorescence in mesophotic reefs, although well described for shallow waters, remains largely unstudied. We found that representatives of many scleractinian species are brightly fluorescent at depths of 50–60 m at the Interuniversity Institute for Marine Sciences (IUI) reef in Eilat, Israel. Some of these fluorescent species have distribution maxima at mesophotic depths (40–100 m). Several individuals from these depths displayed yellow or orange-red fluorescence, the latter being essentially absent in corals from the shallowest parts of this reef. We demonstrate experimentally that in some cases the production of fluorescent pigments is independent of the exposure to light; while in others, the fluorescence signature is altered or lost when the animals are kept in darkness. Furthermore, we show that green-to-red photoconversion of fluorescent pigments mediated by short-wavelength light can occur also at depths where ultraviolet wavelengths are absent from the underwater light field. Intraspecific colour polymorphisms regarding the colour of the tissue fluorescence, common among shallow water corals, were also observed for mesophotic species. Our results suggest that fluorescent pigments in mesophotic reefs fulfil a distinct biological function and offer promising application potential for coral-reef monitoring and biomedical imaging

Metabolic networking in Brunfelsia calycina petals after flower opening

Brunfelsia calycina flowers change colour from purple to white due to anthocyanin degradation, parallel to an increase in fragrance and petal size. Here it was tested whether the production of the fragrant benzenoids is dependent on induction of the shikimate pathway, or if they are formed from the anthocyanin degradation products. An extensive characterization of the events taking place in Brunfelsia flowers is presented. Anthocyanin characterization was performed using ultraperfomance liquid chromatography–quadrupole time of flight–tandem mass specrometry (UPLC-QTOF-MS/MS). Volatiles emitted were identified by headspace solid phase microextraction–gas chromatography–mass spectrometry (HS-SPME-GC-MS). Accumulated proteins were identified by 2D gel electrophoresis. Transcription profiles were characterized by cross-species hybridization of Brunfelsia cDNAs to potato cDNA microarrays. Identification of accumulated metabolites was performed by UPLC-QTOF-MS non-targeted metabolite analysis. The results include characterization of the nine main anthocyanins in Brunfelsia flowers. In addition, 146 up-regulated genes, 19 volatiles, seven proteins, and 17 metabolites that increased during anthocyanin degradation were identified. A multilevel analysis suggests induction of the shikimate pathway. This pathway is the most probable source of the phenolic acids, which in turn are precursors of both the benzenoid and lignin production pathways. The knowledge obtained is valuable for future studies on degradation of anthocyanins, formation of volatiles, and the network of secondary metabolism in Brunfelsia and related species

Reciprocal-transplantation between shallow and mesophotic stony corals

Most studies to date on the various life-history aspects of scleractinian corals (e.g. reproduction, connectivity, and physiology) have focused on their innate habitats. However, comprehensive data on the ability of both shallow and mesophotic corals to contend in the coming decades with the different environmental conditions they may encounter due to new habitats or environmental changes (e.g. eutrophication), are scarce. Long-term cross-transplantation experiments assessing the potential responses and acclimatization ability of corals are thus needed in order to expand our knowledge. Here we examined the survivorship and changes in the photobiological acclimatization of corals following their cross-transplantation between two different depths (5–10 m and 45 m) and two sites characterized by different abiotic conditions (i.e. light, nutrient, and sedimentation regime). This year-long in-situ experiment was performed on five depth-generalist coral species. Depth of origin and the species’ particular morphology were found to be the strongest predictors of survivorship. Physiological responses occurred mainly among those corals that had been translocated from deep-to-shallow water, and were expressed in a significant reduction in chlorophyll-a concentration and algal density, as well as changes in photosynthetic parameters (e.g. minimal/maximal saturating points, Ek and Em, and rETRmax). Our study contributes to a better assessment of the physiological and ecological consequences of corals under acute and long-term environmental perturbations and their endurance abilities. Furthermore, it contributes to the information necessary for effective management intervention aimed at supporting the possible acclimation or rehabilitation of coral species

Data from: Photoacclimation and induction of light-enhanced calcification in the mesophotic coral Euphyllia paradivisa

Corals and their photosymbionts experience inherent changes in light along depth gradients, leading them to have evolved several well-investigated photoacclimation strategies. As coral calcification is influenced by light (a process described as LEC-“light enhanced calcification”), studies have sought to determine the link between photosynthesis and calcification, but many puzzling aspects still persist. Here we examine the physiology of Euphyllia paradivisa, a coral species found at a wide range of depths but that is strictly mesophotic in the Red Sea; and also examines the coupling between photosynthesis and light-enhanced calcification by investigating the response of the coral under several controlled light regimes during a long-term experiment. E. paradivisa specimens were collected from 40-50 m depth and incubated under three light conditions for a period of one year: full-spectrum shallow-water light (~3 m, e.g. shallow-light treatment); blue deep-water light (~40 m, e.g. mesophotic-light treatment); or total darkness (e.g. dark treatment). Net photosynthesis remained similar in the shallow-light treated corals compared to the mesophotic-light treated corals, under both low and high light. However, calcification increased dramatically with increasing light intensity in the shallow-light treated corals suggesting a decoupling between these processes. Photoacclimation to shallow-water conditions was indicated by enhanced respiration, a higher density of zooxanthellae per polyp, and lower chlorophyll a content per cell. The dark-treated corals became completely bleached but did not lower their metabolism below that of the mesophotic-light treated corals. No Symbiodinium clade shift was found following the year-long light treatments. We conclude that E. paradivisa, and its original symbiont clade, can adapt to various light conditions by controlling its metabolic rate and growth energy investment, and consequently induce LEC

Repetitive sex change in the stony coral Herpolitha limax across a wide geographic range

Sex change has been widely studied in animals and plants. However, the conditions favoring sex change, its mode and timing remain poorly known. Here, for the first time in stony corals, we report on a protandrous (youngest individuals are males) repetitive sex change exhibited by the fungiid coral Herpolitha limax across large spatial scales (the coral reefs of Japan, Jordan and Israel) and temporal scales (2004–2017). In contrast to most corals, this species is a daytime spawner (08:00–10:00 AM) that spawned at the same time/same date across all the study sites. The sporadically scattered populations of H. limax among the coral reefs of Eilat (Israel) and Aqaba (Jordan) exhibited significantly slower growth, earlier sex change, and lower percentages of reproduction and sex change in comparison to the densely aggregated populations in Okinawa (Japan). At all sites, sex ratio varied among years, but was almost always biased towards maleness. Growth rate decreased with size. We conclude that comparable to dioecious plants that display labile sexuality in response to energetic and/or environmental constraints, the repetitive sex change displayed by H. limax increases its overall fitness reinforcing the important role of reproductive plasticity in the Phylum Cnidaria in determining their evolutionary success

ESM 2 - Photosynthesis and calcification

Supporting dat

Biogeography, reproductive biology and phylogenetic divergence within the Fungiidae (mushroom corals)

While the escalating impacts of climate change and other anthropogenic pressures on coral reefs are well documented at the coral community level, studies of species-specific trends are less common, owing mostly to the difficulties and uncertainties in delineating coral species. It has also become clear that traditional coral taxonomy based largely on skeletal macromorphology has underestimated the diversity of many coral families. Here, we use targeted enrichment methods to sequence 2476 ultraconserved elements (UCEs) and exonic loci to investigate the relationship between populations of Fungia fungites from Okinawa, Japan, where this species reproduces by brooding (i.e., internal fertilization), and Papua New Guinea and Australia, where it reproduces by broadcast-spawning (i.e., external fertilization). Moreover, we analyzed the relationships between populations of additional fungiid species (Herpolitha limax and Ctenactis spp.) that reproduce only by broadcast-spawning. Our phylogenetic and species delimitation analyses reveal strong biogeographic structuring in both F. fungites and Herpolitha limax, consistent with cryptic speciation in Okinawa in both species and additionally for H. limax in the Red Sea. By combining UCE/exon data and mitochondrial sequences captured in off-target reads, we reinforce earlier findings that Ctenactis, a genus consisting of three nominal morphospecies, is not a natural group. Our results highlight the need for taxonomic and systematic re-evaluations of some species and genera within the family Fungiidae. This work demonstrates that sequence data generated by the application of targeted capture methods can provide objective criteria by which we can test phylogenetic hypotheses based on morphological and/or life history traits

Selective deep water coral bleaching occurs through depth isolation

Climate change is degrading coral reefs around the world. Mass coral bleaching events have become more frequent in recent decades, leading to dramatic declines in coral cover. Mesophotic coral ecosystems (30–150 m depth) comprise an estimated 50–80 % of global coral reef area. The potential for these to act as refuges from climate change is unresolved. Here, we report three mesophotic-specific coral bleaching events in the northern Red Sea over the course of eight years. Over the last decade, faster temperature increases at mesophotic depths resulted in ~50 % decline in coral populations, while the adjacent shallow coral reefs remained intact. Further, community structure shifted from hard coral dominated to turf algae dominated throughout these recurrent bleaching events. Our results do not falsify the notion of the northern Red Sea as a thermal refuge for shallow coral reefs, but question the capacity of mesophotic ecosystems to act as a universal tropical refuge