Reef-building corals farm and feed on their photosynthetic symbionts.

Coral reefs are highly diverse ecosystems that thrive in nutrient-poor waters, a phenomenon frequently referred to as the Darwin paradox1. The energy demand of coral animal hosts can often be fully met by the excess production of carbon-rich photosynthates by their algal symbionts2,3. However, the understanding of mechanisms that enable corals to acquire the vital nutrients nitrogen and phosphorus from their symbionts is incomplete4-9. Here we show, through a series of long-term experiments, that the uptake of dissolved inorganic nitrogen and phosphorus by the symbionts alone is sufficient to sustain rapid coral growth. Next, considering the nitrogen and phosphorus budgets of host and symbionts, we identify that these nutrients are gathered through symbiont 'farming' and are translocated to the host by digestion of excess symbiont cells. Finally, we use a large-scale natural experiment in which seabirds fertilize some reefs but not others, to show that the efficient utilization of dissolved inorganic nutrients by symbiotic corals established in our laboratory experiments has the potential to enhance coral growth in the wild at the ecosystem level. Feeding on symbionts enables coral animals to tap into an important nutrient pool and helps to explain the evolutionary and ecological success of symbiotic corals in nutrient-limited waters.

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.

Coral fluorescence: a prey-lure in deep habitats.

Fluorescence is highly prevalent in reef-building corals, nevertheless its biological role is still under ongoing debate. This feature of corals was previously suggested to primarily screen harmful radiation or facilitate coral photosynthesis. In mesophotic coral ecosystems (MCEs; 30-150 m depth) corals experience a limited, blue-shifted light environment. Consequently, in contrast to their shallow conspecifics, they might not be able to rely on photosynthates from their photosymbionts as their main energy source. Here, we experimentally test an alternative hypothesis for coral fluorescence: a prey-lure mechanism for plankton. We show that plankton exhibit preferential swimming towards green fluorescent cues and that compared to other morphs, higher predation rates are recorded in a green fluorescing morph of the mesophotic coral Euphyllia paradivisa. The evidence provided here - that plankton are actively attracted to fluorescent signals - indicates the significant role of fluorescence in amplifying the nutritional sink adjacent to coral reefs.

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.

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.

Response of fluorescence morphs of the mesophotic coral Euphyllia paradivisa to ultra-violet radiation.

Euphyllia paradivisa is a strictly mesophotic coral in the reefs of Eilat that displays a striking color polymorphism, attributed to fluorescent proteins (FPs). FPs, which are used as visual markers in biomedical research, have been suggested to serve as photoprotectors or as facilitators of photosynthesis in corals due to their ability to transform light. Solar radiation that penetrates the sea includes, among others, both vital photosynthetic active radiation (PAR) and ultra-violet radiation (UVR). Both types, at high intensities, are known to have negative effects on corals, ranging from cellular damage to changes in community structure. In the present study, fluorescence morphs of E. paradivisa were used to investigate UVR response in a mesophotic organism and to examine the phenomenon of fluorescence polymorphism. E. paradivisa, although able to survive in high-light environments, displayed several physiological and behavioral responses that indicated severe light and UVR stress. We suggest that high PAR and UVR are potential drivers behind the absence of this coral from shallow reefs. Moreover, we found no significant differences between the different fluorescence morphs' responses and no evidence of either photoprotection or photosynthesis enhancement. We therefore suggest that FPs in mesophotic corals might have a different biological role than that previously hypothesized for shallow corals.

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 LEC by investigating the response of the coral under several controlled light regimes during a long-term experiment. E. paradivisa specimens were collected from 40 to 50 m depth and incubated under three light conditions for a period of 1 year: full-spectrum shallow-water light (approx. 3 m, e.g. shallow-light treatment); blue deep-water light (approx. 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.

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.