Impacts of ocean warming on fish size reductions on the world's hottest coral reefs.

The impact of ocean warming on fish and fisheries is vigorously debated. Leading theories project limited adaptive capacity of tropical fishes and 14-39% size reductions by 2050 due to mass-scaling limitations of oxygen supply in larger individuals. Using the world's hottest coral reefs in the Persian/Arabian Gulf as a natural laboratory for ocean warming - where species have survived >35.0 °C summer temperatures for over 6000 years and are 14-40% smaller at maximum size compared to cooler locations - we identified two adaptive pathways that enhance survival at elevated temperatures across 10 metabolic and swimming performance metrics. Comparing Lutjanus ehrenbergii and Scolopsis ghanam from reefs both inside and outside the Persian/Arabian Gulf across temperatures of 27.0 °C, 31.5 °C and 35.5 °C, we reveal that these species show a lower-than-expected rise in basal metabolic demands and a right-shifted thermal window, which aids in maintaining oxygen supply and aerobic performance to 35.5 °C. Importantly, our findings challenge traditional oxygen-limitation theories, suggesting a mismatch in energy acquisition and demand as the primary driver of size reductions. Our data support a modified resource-acquisition theory to explain how ocean warming leads to species-specific size reductions and why smaller individuals are evolutionarily favored under elevated temperatures.

Unraveling the predictive role of temperature in the gut microbiota of the sea urchin Echinometra sp. EZ across spatial and temporal gradients.

Shifts in microbial communities represent a rapid response mechanism for host organisms to respond to changes in environmental conditions. Therefore, they are likely to be important in assisting the acclimatization of hosts to seasonal temperature changes as well as to variation in temperatures across a species' range. The Persian/Arabian Gulf is the world's warmest sea, with large seasonal fluctuations in temperature (20℃ - 37℃) and is connected to the Gulf of Oman which experiences more typical oceanic conditions (<32℃ in the summer). This system is an informative model for understanding how symbiotic microbial assemblages respond to thermal variation across temporal and spatial scales. Here, we elucidate the role of temperature on the microbial gut community of the sea urchin Echinometra sp. EZ and identify microbial taxa that are tightly correlated with the thermal environment. We generated two independent datasets with a high degree of geographic and temporal resolution. The results show that microbial communities vary across thermally variable habitats, display temporal shifts that correlate with temperature, and can become more disperse as temperatures rise. The relative abundances of several ASVs significantly correlate with temperature in both independent datasets despite the >300 km distance between the furthest sites and the extreme seasonal variations. Notably, over 50% of the temperature predictive ASVs identified from the two datasets belonged to the family Vibrionaceae. Together, our results identify temperature as a robust predictor of community-level variation and highlight specific microbial taxa putatively involved in the response to thermal environment.

Population Genomic Analyses of the Sea Urchin Echinometra sp. EZ across an Extreme Environmental Gradient.

Extreme environmental gradients represent excellent study systems to better understand the variables that mediate patterns of genomic variation between populations. They also allow for more accurate predictions of how future environmental change might affect marine species. The Persian/Arabian Gulf is extreme in both temperature and salinity, whereas the adjacent Gulf of Oman has conditions more typical of tropical oceans. The sea urchin Echinometra sp. EZ inhabits both of these seas and plays a critical role in coral reef health as a grazer and bioeroder, but, to date, there have been no population genomic studies on this or any urchin species in this unique region. E sp. EZ's life history traits (e.g., large population sizes, large reproductive clutches, and long life spans), in theory, should homogenize populations unless nonneutral processes are occurring. Here, we generated a draft genome and a restriction site-associated DNA sequencing data set from seven populations along an environmental gradient across the Persian/Arabian Gulf and the Gulf of Oman. The estimated genome size of E. sp. EZ was 609 Mb and the heterozygosity was among the highest recorded for an echinoderm at 4.5%. We recovered 918 high-quality SNPs from 85 individuals which we then used in downstream analyses. Population structure analyses revealed a high degree of admixture between all sites, although there was population differentiation and significant pairwise FST values between the two seas. Preliminary results suggest migration is bidirectional between the seas and nine candidate loci were identified as being under putative natural selection, including one collagen gene. This study is the first to investigate the population genomics of a sea urchin from this extreme environmental gradient and is an important contribution to our understanding of the complex spatial patterns that drive genomic divergence.

Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility.

Reef-building corals are at risk of extinction from ocean warming. While some corals can enhance their thermal limits by associating with dinoflagellate photosymbionts of superior stress tolerance, the extent to which symbiont communities will reorganize under increased warming pressure remains unclear. Here we show that corals in the hottest reefs in the world in the Persian Gulf maintain associations with the same symbionts across 1.5 years despite extreme seasonal warming and acute heat stress (≥35°C). Persian Gulf corals predominantly associated with Cladocopium (clade C) and most also hosted Symbiodinium (clade A) and/or Durusdinium (clade D). This is in contrast to the neighbouring and milder Oman Sea, where corals associated with Durusdinium and only a minority hosted background levels of Cladocopium. During acute heat stress, the higher prevalence of Symbiodinium and Durusdinium in bleached versus nonbleached Persian Gulf corals indicates that genotypes of these background genera did not confer bleaching resistance. Within symbiont genera, the majority of ITS2 rDNA type profiles were unique to their respective coral species, confirming the existence of host-specific symbiont lineages. Notably, further differentiation among Persian Gulf sites demonstrates that symbiont populations are either isolated or specialized over tens to hundreds of kilometres. Thermal tolerance across coral species was associated with the prevalence of a single ITS2 intragenomic sequence variant (C3gulf), definitive of the Cladocopium thermophilum group. The abundance of C3gulf was highest in bleaching-resistant corals and at warmer sites, potentially indicating a specific symbiont genotype (or set of genotypes) that may play a role in thermal tolerance that warrants further investigation. Together, our findings indicate that co-evolution of host-Symbiodiniaceae partnerships favours fidelity rather than flexibility in extreme environments and under future warming.

The changing dynamics of coral reef science in Arabia.

Six percent of the world's coral reefs occur around the Arabian Peninsula, providing a valuable ecological, economic and scientific resource for the nations bordering its shores. We provide the first region-wide assessment of the current status and historical trends in coral reef research, focusing on research in the Red Sea, Arabian Sea, and Arabian Gulf. In total, 633 regional reef publications have been produced since the 1930s, covering a wide variety of themes and taxa. Our results show a great deal of commonality in regional reef research, but also highlight important differences in research among the various seas as well as knowledge gaps that represent opportunities for future research. A regionally-integrated approach to future research is essential. There is a growing need for large-scale research to guide management of reefs and their stressors, as these operate at much larger scales than the national borders within which most research currently occurs.

Levels of genetic diversity and taxonomic status of Epinephelus species in United Arab Emirates fish markets.

Understanding the patterns of genetic diversity of fish species is essential for marine conservation and management. This is particularly important in the Arabian Gulf where marine life is subject to extreme environmental conditions that could impact genetic diversity. Here we assess genetic diversity of the most commercially important fish in the United Arab Emirates; groupers (Epinephelus spp.). Sequencing of 973 bp mitochondrial DNA from 140 tissue samples collected in four main fish markets revealed 58 haplotypes clustered within three groups. Data analysis revealed the presence of three distinct Epinephelus species being marketed as one species (hammour): Epinephelus coioides, Epinephelus areolatus and Epinephelus bleekeri. We report species-specific genetic markers and demonstrate that all three species exhibit relatively low levels of genetic variation, reflecting the effect of overfishing and environmental pressures. In light of the genetic evidence presented here, conservation and management of groupers in the UAE warrant the implementation of species-specific measures.