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.

Assessment of storm impact on coral reef structural complexity.

Extreme weather events are increasing in frequency and magnitude. Consequently, it is important to understand their effects and remediation. Resilience reflects the ability of an ecosystem to absorb change, which is important for understanding ecological dynamics and trajectories. To describe the impact of a powerful storm on coral reef structural complexity, we used novel computational tools and detailed 3D reconstructions captured at three time points over three years. Our data-set Reefs4D of 21 co-registered image-based models enabled us to calculate the differences at seven sites over time and is released with the paper. We employed six geometrical metrics, two of which are new algorithms for calculating fractal dimension of reefs in full 3D. We conducted a multivariate analysis to reveal which sites were affected the most and their relative recovery. We also explored the changes in fractal dimension per size category using our cube-counting algorithm. Three metrics showed a significant difference between time points, i.e., decline and subsequent recovery in structural complexity. The multivariate analysis and the results per size category showed a similar trend. Coral reef resilience has been the subject of seminal studies in ecology. We add important information to the discussion by focusing on 3D structure through image-based modeling. The full picture shows resilience in structural complexity, suggesting that the reef has not gone through a catastrophic phase shift. Our novel analysis framework is widely transferable and useful for research, monitoring, and management.

Light pollution alters the skeletal morphology of coral juveniles and impairs their light capture capacity.

Urbanization and infrastructure development have changed the night-time light regime of many coastal marine habitats. Consequently, Artificial Light at Night (ALAN) is becoming a global ecological concern, particularly in nearshore coral reef ecosystems. However, the effects of ALAN on coral architecture and their optical properties are unexplored. Here, we conducted a long-term ex situ experiment (30 months from settlement) on juvenile Stylophora pistillata corals grown under ALAN conditions using light-emitting diodes (LEDs) and fluorescent lamps, mimicking light-polluted habitats. We found that corals exposed to ALAN exhibited altered skeletal morphology that subsequently resulted in reduced light capture capacity, while also gaining better structural and optical modifications to increased light levels than their ambient-light counterparts. Additionally, light-polluted corals developed a more porous skeleton compared to the control corals. We suggest that ALAN induces light stress in corals, leading to a decrease in the solar energy available for photosynthesis during daytime illumination.

Coming of age: Annual onset of coral reproduction is determined by age rather than size.

Constraints on organisms possessing a unitary body plan appear almost absent from colonial organisms. Like unitary organisms, however, coral colonies seemingly delay reproduction until reaching a critical size. Elucidating ontogenetic processes, such as puberty and aging are complicated by corals' modular design, where partial mortality and fragmentation lead to distortions in colony size-age relationships. We explored these enigmatic relations and their influence on reproduction by fragmenting sexually mature colonies of five coral species into sizes below the known size at first reproduction, nurturing them for prolonged periods, and examining their reproductive capacity and trade-offs between growth rates and reproductive investment. Most fragments were reproductive regardless of their size, and growth rates hardly affected reproduction. Our findings suggest that once the ontogenetic milestone of puberty is reached, corals retain reproductive capacity irrespective of colony size, highlighting the key role that aging may have in colonial animals, which are commonly considered non-aging.

Morpho-functional traits of the coral Stylophora pistillata enhance light capture for photosynthesis at mesophotic depths.

The morphological architecture of photosynthetic corals modulates the light capture and functioning of the coral-algal symbiosis on shallow-water corals. Since corals can thrive on mesophotic reefs under extreme light-limited conditions, we hypothesized that microskeletal coral features enhance light capture under low-light environments. Utilizing micro-computed tomography scanning, we conducted a novel comprehensive three-dimensional (3D) assessment of the small-scale skeleton morphology of the depth-generalist coral Stylophora pistillata collected from shallow (4-5 m) and mesophotic (45-50 m) depths. We detected a high phenotypic diversity between depths, resulting in two distinct morphotypes, with calyx diameter, theca height, and corallite marginal spacing contributing to most of the variation between depths. To determine whether such depth-specific morphotypes affect coral light capture and photosynthesis on the corallite scale, we developed 3D simulations of light propagation and photosynthesis. We found that microstructural features of corallites from mesophotic corals provide a greater ability to use solar energy under light-limited conditions; while corals associated with shallow morphotypes avoided excess light through self-shading skeletal architectures. The results from our study suggest that skeleton morphology plays a key role in coral photoadaptation to light-limited environments.

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.

Soft coral reproductive phenology along a depth gradient: Can "going deeper" provide a viable refuge?

Many species across a wide range of taxa and habitats display phenological shifts and differences in response to both environmental gradients and climate change. Moreover, the wide-scale decline of numerous ecosystems is leading to increasing efforts to identify zones that might serve as natural refuges from various disturbances, including ocean warming. One such refuge was suggested to be that of the deep coral reefs, but whether depth can provide coral populations with a viable and reproductive refuge remains unclear. Given the global coral-reef degradation and the key role that corals play as ecosystem engineers, their reproductive ecology has been widely studied. A particular knowledge gap nonetheless exists regarding coral reproductive phenology along a depth gradient. Filling in this gap may uncover the environmental cues that regulate coral reproduction, leading to better predictions of population connectivity, and their possible responses to climate change and other environmental changes. Here, using long-term in situ observations of the soft coral Rhytisma fulvum's reproductive activity along its entire depth range (0-45 m), we examined the relationship among several environmental factors and the coral's reproductive phenology and activity over five successive annual breeding seasons. Compared with the shallow depths, a lower number of reproducing colonies was found in habitats deeper than 30 m, highlighting possible constraints on coral reproduction at the deeper end of their range. Our results further revealed that an increase in seawater temperature over 1-2-day intervals during the breeding season correlated with the onset of reproductive activity along the depth gradient, leading to different reproductive periodicities in different depths. These differences suggest that differential temperature regimes and reproductive timing across depth may create intraspecific temporal reproductive segregation, possibly reducing connectivity among populations along a depth gradient. Moreover, we found high variability among years in both the timing of breeding activities and in the level of reproductive synchrony among corals from different depths. Overall, our study questions whether depth can provide a long-term and viable refuge for corals in the face of global environmental changes.

Emerging 3D technologies for future reformation of coral reefs: Enhancing biodiversity using biomimetic structures based on designs by nature.

The rapid decline of vulnerable coral reefs has increased the necessity of exploring interdisciplinary methods for reef restoration. Examining how to upgrade these tools may uncover options to better support or increase biodiversity of coral reefs. As many of the issues facing reef restoration today deal with the scalability and effectiveness of restoration efforts, there is an urgency to invest in technology that can help reach ecosystem-scale. Here, we provide an overview on the evolution to current state of artificial reefs as a reef reformation tool and discuss a blueprint with which to guide the next generation of biomimetic artificial habitats for ecosystem support. Currently, existing artificial structures have difficulty replicating the 3D complexity of coral habitats and scaling them to larger areas can be problematic in terms of production and design. We introduce a novel customizable 3D interface for producing scalable, biomimetic artificial structures, utilizing real data collected from coral ecosystems. This interface employs 3D technologies, 3D imaging and 3D printing, to extract core reef characteristics, which can be translated and digitized into a 3D printed artificial reef. The advantages of 3D printing lie in providing customized tools by which to integrate the vital details of natural reefs, such as rugosity and complexity, into a sustainable manufacturing process. This methodology can offer economic solutions for developing both small and large-scale biomimetic structures for a variety of restoration situations, that closely resemble the coral reefs they intend to support.

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.

Depth-dependent parental effects create invisible barriers to coral dispersal.

Historically, marine populations were considered to be interconnected across large geographic regions due to the lack of apparent physical barriers to dispersal, coupled with a potentially widely dispersive pelagic larval stage. Recent studies, however, are providing increasing evidence of small-scale genetic segregation of populations across habitats and depths, separated in some cases by only a few dozen meters. Here, we performed a series of ex-situ and in-situ experiments using coral larvae of three brooding species from contrasting shallow- and deep-water reef habitats, and show that their settlement success, habitat choices, and subsequent survival are substantially influenced by parental effects in a habitat-dependent manner. Generally, larvae originating from deep-water corals, which experience less variable conditions, expressed more specific responses than shallow-water larvae, with a higher settlement success in simulated parental-habitat conditions. Survival of juvenile corals experimentally translocated to the sea was significantly lower when not at parental depths. We conclude that local adaptations and parental effects alongside larval selectivity and phenotype-environment mismatches combine to create invisible semipermeable barriers to coral dispersal and connectivity, leading to habitat-dependent population segregation.

Population dynamics and growth rates of free-living mushroom corals (Scleractinia: Fungiidae) in the sediment-stressed reefs of Singapore.

The reefs of Singapore provide an excellent opportunity to study the population dynamics and growth rates of free-living mushroom corals (Fungiidae) under sediment-stressed conditions. Transect surveys at four study sites revealed a total of 11 free-living mushroom coral species-the same 11 species as those found by local studies since the 1980s. The abundance of the four most common species ranged from 1.0 to 68.3 Ind. per 100m2, while their population size-structure showed a common pattern of a higher proportion of small-sized corals than large-sized ones (i.e. positively skewed size-structure), although very few individuals of the smallest-size classes were recorded for any of the four species. A more positively skewed size-structure for each of the four most common species was observed at the reef slope (5-6m depth) than at the reef crest (2-3m depth), possibly due to a slower growth rate caused by light reduction with depth. All the mushroom corals studied exhibited a decline in growth rate with increasing size and weight, indicating determinate growth. Growth rate of each of the four most common species was similar among the study sites, despite variation in environmental conditions. Our results demonstrate species richness stability over the past three decades, suggesting that these free-living mushroom coral assemblages comprise species that are well-adapted to the chronic high sedimentation characteristic of Singapore's reefs. However, if the paucity of individuals of the smallest-size classes reflects poor recruitment and/or early mortality, there may be some cause for concern. Our robust baseline data can contribute to a long-term monitoring strategy for determination of changes in mushroom coral population dynamics.

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.

The Complexity of the Holobiont in the Red Sea Coral Euphyllia paradivisa under Heat Stress.

The recognition of the microbiota complexity and their role in the evolution of their host is leading to the popularization of the holobiont concept. However, the coral holobiont (host and its microbiota) is still enigmatic and unclear. Here, we explore the complex relations between different holobiont members of a mesophotic coral Euphyllia paradivisa. We subjected two lines of the coral-with photosymbionts, and without photosymbionts (apo-symbiotic)-to increasing temperatures and to antibiotics. The different symbiotic states were characterized using transcriptomics, microbiology and physiology techniques. The bacterial community's composition is dominated by bacteroidetes, alphaproteobacteria, and gammaproteobacteria, but is dependent upon the symbiont state, colony, temperature treatment, and antibiotic exposure. Overall, the most important parameter determining the response was whether the coral was a symbiont/apo-symbiotic, while the colony and bacterial composition were secondary factors. Enrichment Gene Ontology analysis of coral host's differentially expressed genes demonstrated the cellular differences between symbiotic and apo-symbiotic samples. Our results demonstrate the significance of each component of the holobiont consortium and imply a coherent link between them, which dramatically impacts the molecular and cellular processes of the coral host, which possibly affect its fitness, particularly under environmental stress.

Effects of Light Pollution on the Early Life Stages of the Most Abundant Northern Red Sea Coral.

The growth in human population along coastal areas is exposing marine environments to increasing anthropogenic light sources. Despite the potential effects of this modern phenomenon, very few studies have examined its implications for corals. Here, we present a long-term study of coral early life stages under light pollution conditions at night. Coral larvae were collected from Stylophora pistillata colonies, and then settled and grown under experimental conditions of two different common city lighting methods (fluorescent or LED). Effects of the artificial lighting on the coral settlement success, survivorship, growth rate, photosynthetic efficiency, and calcification rate were examined over a period of one year. The control exhibited ~30% higher settlement success compared to the two light treatments, while under the light treatments corals showed higher survivorship, growth, and calcification rates. In addition, an indication of damage to the photosynthetic system was found in the light-polluted corals, which was reflected in their photosynthesis efficiency parameters: i.e., lower maximum light utilization coefficient (α), lower maximum potential photosynthetic rate (Pmax), and lower photosynthetic maximal quantum yield (Fv/Fm). Our findings provide evidence of the potential adverse effects of artificial lighting methods on the natural environment of coral reefs. We conclude that the use of the LED lighting method has high interference potential for the early life stages of corals.

Breakdown in spawning synchrony: A silent threat to coral persistence.

The impacts of human and natural disturbances on coral reefs are typically quantified through visible damage (e.g., reduced coral coverage as a result of bleaching events), but changes in environmental conditions may also cause damage in less visible ways. Despite the current paradigm, which suggests consistent, highly synchronized spawning events, corals that reproduce by broadcast spawning are particularly vulnerable because their reproductive phenology is governed by environmental cues. Here, we quantify coral spawning intensity during four annual reproductive seasons, alongside laboratory analyses at the polyp, colony, and population levels, and we demonstrate that, compared with historical data, several species from the Red Sea have lost their reproductive synchrony. Ultimately, such a synchrony breakdown reduces the probability of successful fertilization, leading to a dearth of new recruits, which may drive aging populations to extinction.

The Algal Symbiont Modifies the Transcriptome of the Scleractinian Coral Euphyllia paradivisa During Heat Stress.

The profound mutualistic symbiosis between corals and their endosymbiotic counterparts, Symbiodiniaceae algae, has been threatened by the increase in seawater temperatures, leading to breakdown of the symbiotic relationship-coral bleaching. To characterize the heat-stress response of the holobiont, we generated vital apo-symbiotic Euphylliaparadivisa corals that lacked the endosymbiotic algae. Using RNA sequencing, we analyzed the gene expression of these apo-symbionts vs. symbiotic ones, to test the effect of the algal presence on the tolerance of the coral. We utilized literature-derived lists of "symbiosis differentially expressed genes" and "coral heat-stress genes" in order to compare between the treatments. The symbiotic and apo-symbiotic samples were segregated into two separate groups with several different enriched gene ontologies. Our findings suggest that the presence of endosymbionts has a greater negative impact on the host than the environmental temperature conditions experienced by the holobiont. The peak of the stress reaction was identified as 28 °C, with the highest number of differentially expressed genes. We suggest that the algal symbionts increase coral holobiont susceptibility to elevated temperatures. Currently, we can only speculate whether coral species, such as E.paradivisa, with the plasticity to also flourish as apo-symbionts, may have a greater chance to withstand the upcoming global climate change challenge.

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.

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.

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.