Extreme environmental conditions reduce coral reef fish biodiversity and productivity

This research investigates the factors influencing species distribution and the impact of resulting assemblages on ecological processes, particularly relevant given the increasing human impact on biodiversity and ecosystem services. A species' presence is determined by a complex interplay of organismal traits (e.g., temperature tolerance, trophic niche), environmental conditions (e.g., temperature, salinity, dissolved oxygen), biotic interactions (habitat or food availability), biogeographic history, and stochastic events. Species diversity directly affects ecosystem functioning, including productivity, and climate change significantly alters these dynamics by modifying abiotic conditions, species niches, and biotic interactions. Changes in environmental factors like temperature affect ectotherms' physiological processes, altering energy expenditure, resource acquisition, and energy allocation. These energy dynamics are fundamental to community assembly and the rates of ecological processes within ecosystems. Coral reefs, the most diverse marine ecosystem, provide vital services, but their foundation species (scleractinian corals) are highly sensitive to thermal extremes, leading to global decline. Consequent decline or shifts in reef fish communities directly impact human reliance on reef fisheries. While some fish species may cope with or even benefit from coral loss, many tropical reef fishes are adapted to narrow environmental conditions and may be directly vulnerable to climate change, especially temperature increases. Temperature is the most commonly studied environmental stressor for reef fishes, with non-lethal adverse physiological, developmental, or behavioral responses often observed outside their normal temperature range. While transgenerational plasticity might enhance offspring performance in higher temperatures, its effectiveness in competitive, uncontrolled environments remains unclear. Cryptobenthic fishes, the smallest reef fishes, are exceptionally suitable for tracing the effects of environmental change. Their small size, high metabolism, and limited mobility suggest high susceptibility to temperature fluctuations. However, their rapid generational turnover and reproductive strategies might also facilitate transgenerational adaptation. This study quantifies cryptobenthic community structure, physiological and dietary traits, and contributions to ecosystem functioning in the Arabian Gulf (world's hottest coral reef environment) and compares it with the Gulf of Oman to understand the impact of extreme conditions on these organisms.

The study draws on existing literature on species distribution, community assembly theory, the effects of climate change on marine ecosystems, particularly coral reefs and reef fish, and the specific challenges faced by cryptobenthic fishes. The authors cite numerous studies on temperature tolerance in reef fishes, transgenerational plasticity, and the role of cryptobenthic fishes in coral reef trophodynamics. They also reference research on the Arabian Gulf's unique environmental conditions and the long-term persistence of corals in this extreme habitat, setting the stage for their investigation into the resilience and adaptive capacity of cryptobenthic fish communities under these harsh conditions.

The study compared cryptobenthic fish assemblages in the southeastern Arabian Gulf (extremely hot temperatures) and the Gulf of Oman (more moderate temperatures). Six reefs, three in each location, were sampled in April and May 2018 using enclosed clove-oil stations. This involved covering a reef outcrop with a net, introducing clove oil to anesthetize the fish, and then collecting all fish within the area. Benthic community structure was assessed using photographs of haphazardly placed quadrats. For thermal tolerance analysis, roving diver collections were conducted to gather a subset of individuals for critical thermal maximum (CTmax) and minimum (CTmin) trials. Fish were gradually exposed to increasing/decreasing water temperatures until loss of equilibrium. Gut content DNA metabarcoding was performed on a subset of individuals from both locations using COI and 23S rRNA gene regions to analyze prey diversity and composition. Length-weight relationships and Bayesian linear models were used to analyze body condition and abundance differences between locations. Finally, individual-based growth and mortality models were used to estimate community-wide biomass cycling metrics (produced biomass, consumed biomass, and turnover). Statistical analyses included Bayesian hierarchical models, nMDS ordination, PERMANOVA, SIMPER, and network analysis to uncover the interplay between environmental variables and organismal characteristics in determining assemblage structures and ecosystem functioning. The data preparation, analysis, and visualization were performed in R using various packages.

Cryptobenthic fish assemblages in the Arabian Gulf showed significantly lower richness (1.62 ± 0.01 SE species m⁻² vs 3.40 ± 0.26 SE species m⁻² in the Gulf of Oman) and abundance (6.12 ± 1.09 SE individuals m⁻² vs 31.94 ± 1.49 SE individuals m⁻²) compared to the Gulf of Oman. However, biomass estimates were comparable. Community composition also differed significantly between locations. Despite comparable benthic composition and live coral cover, the cryptobenthic fish communities were strikingly different. While species-specific critical thermal tolerance limits did not explain the absence of Gulf of Oman species in the Arabian Gulf, population-specific differences in ingested prey and body condition were observed. Gut content metabarcoding revealed strong dietary differences between locations, with Arabian Gulf populations exhibiting lower prey diversity and different prey composition compared to their Gulf of Oman counterparts. Length-weight relationships showed that Gulf of Oman populations of three co-occurring species consistently weighed more for a given body length than their Arabian Gulf counterparts. Modeling of individual-based growth and mortality indicated that biomass production was almost an order of magnitude lower in the Arabian Gulf compared to the Gulf of Oman. Consumed biomass and turnover were also significantly lower in the Arabian Gulf. The Arabian Gulf goby *Coryogalops anomolus* was an exception, showing a higher abundance and similar body condition to the Gulf of Oman population and a less distinct diet between regions, potentially indicating preadaptation to the extreme environment.

The findings suggest that species presence/absence in the Arabian Gulf is not primarily driven by thermal tolerances to short-term temperature extremes, but rather by more nuanced factors such as sublethal physiological effects of temperature and differences in prey resources. The lower body condition and reduced prey diversity in the Arabian Gulf suggest an energetically challenging environment. This 'energetic double jeopardy'—increased energetic costs associated with thermal tolerance adjustments combined with limited and potentially lower-quality prey—likely presents an insurmountable obstacle for many cryptobenthic species. The case of *C. anomolus*, with its less extreme differences in body condition and diet, highlights the potential role of preadaptation via evolutionary processes in enabling persistence in extreme environments. This study contradicts the common focus on immediate, lethal effects of temperature and instead emphasizes the long-term, sublethal effects of environmental extremes.

This research demonstrates that the reduced diversity and abundance of cryptobenthic fishes in the Arabian Gulf are largely driven by energetic limitations rather than direct temperature effects. The energetic costs of adapting to extreme conditions, combined with altered prey availability, pose significant challenges for these small ectotherms. This 'energetic double jeopardy' significantly impacts ecosystem-level productivity, energy transfer, and biomass replenishment. Future research could explore the nutritional quality and energetic densities of prey items, investigate the role of other environmental factors (salinity), and further assess the long-term implications of this energetic filtering effect on coral reef ecosystem functioning under climate change.

The study's sampling was not temporally replicated, so it cannot fully account for potential annual changes in community structures. The assumption of hemispherical reef outcrops in surface area calculations might introduce some error, although it is unlikely to greatly alter the conclusions. Also, while the authors attempt to account for various factors, the complex interplay of variables in the natural environment means that it might not be possible to fully isolate all effects.