Gal Eyal

Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change

Significance Reef corals in the Persian/Arabian Gulf (PAG) withstand exceptionally high salinity and regular summer temperatures of ∼35 °C that kill conspecifics elsewhere. These thermotolerant communities established themselves within only ∼6,000 y under the pressure of rapid climate change and can therefore inform how other coral reefs may respond to global warming. One key to the thermotolerance of PAG corals is their symbiosis with Symbiodinium thermophilum. Phylogeographic evidence indicates that this symbiont represents a stress-tolerant subpopulation of an ancestral taxonomic group with surprising genetic diversity that exists at barely detectable levels outside the PAG. Our results highlight the critical importance of present-day biodiversity for future adaptation to climate change for coral reefs and ecosystems in general. Coral communities in the Persian/Arabian Gulf (PAG) withstand unusually high salinity levels and regular summer temperature maxima of up to ∼35 °C that kill conspecifics elsewhere. Due to the recent formation of the PAG and its subsequent shift to a hot climate, these corals have had only <6,000 y to adapt to these extreme conditions and can therefore inform on how coral reefs may respond to global warming. One key to coral survival in the world’s warmest reefs are symbioses with a newly discovered alga, Symbiodinium thermophilum. Currently, it is unknown whether this symbiont originated elsewhere or emerged from unexpectedly fast evolution catalyzed by the extreme environment. Analyzing genetic diversity of symbiotic algae across >5,000 km of the PAG, the Gulf of Oman, and the Red Sea coastline, we show that S. thermophilum is a member of a highly diverse, ancient group of symbionts cryptically distributed outside the PAG. We argue that the adjustment to temperature extremes by PAG corals was facilitated by the positive selection of preadapted symbionts. Our findings suggest that maintaining the largest possible pool of potentially stress-tolerant genotypes by protecting existing biodiversity is crucial to promote rapid adaptation to present-day climate change, not only for coral reefs, but for ecosystems in general.

Theme section on mesophotic coral ecosystems: advances in knowledge and future perspectives

Abstract The Second International Mesophotic Coral Ecosystems (MCEs) workshop was held in Eilat, Israel, October 26–31, 2014. Here we provide an account of: (1) advances in our knowledge of MCE ecology, including the central question of the potential vertical connectivity between MCEs and shallow-water reefs (SWRs), and that of the validity of the deep-reef refugia hypothesis (DRRH); (2) the contribution of the 2014 MCE workshop to the central question presented in (1), as well as its contribution to novel MCE studies on corals, sponges, fish, and crabs; and (3) gaps, priorities, and recommendations for future research stemming from the workshop. Despite their close proximity to well-studied SWRs, and the growing evidence of their importance, our scientific knowledge of MCEs is still in its infancy. During the last five years, we have witnessed an ever-increasing scientific interest in MCEs, expressed in the exponential increase in the number of publications studying this unique environment. The emerging consensus is that lower MCE benthic assemblages represent unique communities, either of separate species or genetically distinct individuals within species, and any significant support for the DRRH will be limited to upper MCEs. Determining the health and stability of MCEs, their biodiversity, and the degree of genetic connectivity among SWRs and MCEs, will ultimately indicate the ability of MCEs to contribute to the resilience of SWRs and help to guide future management and conservation strategies. MCEs deserve therefore management consideration in their own right. With the technological advancements taking place in recent years that facilitate access to MCEs, the prospects for exciting and innovative discoveries resulting from MCE research, spanning a wide variety of fields, are immense.

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.

Reproduction, abundance and survivorship of two Alveopora spp. in the mesophotic reefs of Eilat, Red Sea.

Although the study of coral reproduction has advanced tremendously over the last few decades, a particular gap exists in our knowledge of the reproductive modes of corals from ‘mesophotic coral ecosystems’ (MCEs) found at 30–150 m depth. Here, we report for the first time on the reproductive patterns, living cover, and survivorship under different light treatments of two scleractinian species from the MCEs of Eilat, Red-Sea: Alveopora allingi and A. ocellata. Both species are found exclusively within MCEs and are high in both abundance and relative cover. These species display a synchronous gametogenic cycles with consecutive oocyte growth and development. Peak of reproductive activity occurs in late summer (September-October), typified by accelerated oocyte growth, coinciding with the rise in seawater temperature. Estimates of fecundity show mean monthly maxima of 48.5 ± 26.3 and 23.5 ± 11.8 (Mean ± SE) oocytes per cm2 for A. allingi and A. ocellata respectively, prior to spawning. A comparison of light and temperature regimes in the shallow vs. MCE environments is presented, and the response of these species to changes in these parameters is discussed. A call encouraging the much-needed studies on the sexuality and reproductive modes of MCE coral species is expressed.

Light-dependent fluorescence in the coral Galaxea fascicularis

Light in the sea is one of the major factors influencing corals, with changes in light being rapid along the depth gradient. Those changes can be a potential stress factor for coral-reef organisms and affect different aspects of the coral’s physiology, including its fluorescence. Fluorescence is a physical phenomenon, comprising the emission of light by a substance that has absorbed light with a different wavelength. Major hypotheses concerning the role of coral fluorescence include that of photoprotection and the facilitation of photosynthesis. We sought to further investigate some ecophysiological aspects of coral fluorescence. We focused on the effect of different light conditions on fluorescence of the coral Galaxea fascicularis and used photography, confocal microscopy, and spectral measurements to assess changes in its fluorescence. We show that fluorescence is significantly influenced by light and, therefore, by depth. Coral fluorescence increased with the increase in light intensity and when the spectrum of light was broader. Hence, we support the “sunscreen” hypothesis and conclude that fluorescence plays a role in the coral’s defense mechanism against harmful radiation. However, multiple fluorescent proteins, as found in different locations of the coral tissue, might suggest more than one functional role of fluorescence in the coral’s physiology.

Improving Automated Annotation of Benthic Survey Images Using Wide-band Fluorescence

Large-scale imaging techniques are used increasingly for ecological surveys. However, manual analysis can be prohibitively expensive, creating a bottleneck between collected images and desired data-products. This bottleneck is particularly severe for benthic surveys, where millions of images are obtained each year. Recent automated annotation methods may provide a solution, but reflectance images do not always contain sufficient information for adequate classification accuracy. In this work, the FluorIS, a low-cost modified consumer camera, was used to capture wide-band wide-field-of-view fluorescence images during a field deployment in Eilat, Israel. The fluorescence images were registered with standard reflectance images, and an automated annotation method based on convolutional neural networks was developed. Our results demonstrate a 22% reduction of classification error-rate when using both images types compared to only using reflectance images. The improvements were large, in particular, for coral reef genera Platygyra, Acropora and Millepora, where classification recall improved by 38%, 33%, and 41%, respectively. We conclude that convolutional neural networks can be used to combine reflectance and fluorescence imagery in order to significantly improve automated annotation accuracy and reduce the manual annotation bottleneck.