A portfolio of climate-tailored approaches to advance the design of marine protected areas in the Red Sea.

Intensified coastal development is compromising the health and functioning of marine ecosystems. A key example of this is the Red Sea, a biodiversity hotspot subjected to increasing local human pressures. While some marine-protected areas (MPAs) were placed to alleviate these stressors, it is unclear whether these MPAs are managed or enforced, thus providing limited protection. Yet, most importantly, MPAs in the Red Sea were not designed using climate considerations, likely diminishing their effectiveness against global stressors. Here, we propose to tailor the design of MPAs in the Red Sea by integrating approaches to enhance climate change mitigation and adaptation. First, including coral bleaching susceptibility could produce a more resilient network of MPAs by safeguarding reefs from different thermal regions that vary in spatiotemporal bleaching responses, reducing the risk that all protected reefs will bleach simultaneously. Second, preserving the basin-wide genetic connectivity patterns that are assisted by mesoscale eddies could further ensure recovery of sensitive populations and maintain species potential to adapt to environmental changes. Finally, protecting mangrove forests in the northern and southern Red Sea that act as major carbon sinks could help offset greenhouse gas emissions. If implemented with multinational cooperation and concerted effort among stakeholders, our portfolio of climate-tailored approaches may help build a network of MPAs in the Red Sea that protects more effectively its coastal resources against escalating coastal development and climate instability. Beyond the Red Sea, we anticipate this study to serve as an example of how to improve the utility of tropical MPAs as climate-informed conservation tools.

Gene expression correlates of social evolution in coral reef butterflyfishes.

Animals display remarkable variation in social behaviour. However, outside of rodents, little is known about the neural mechanisms of social variation, and whether they are shared across species and sexes, limiting our understanding of how sociality evolves. Using coral reef butterflyfishes, we examined gene expression correlates of social variation (i.e. pair bonding versus solitary living) within and between species and sexes. In several brain regions, we quantified gene expression of receptors important for social variation in mammals: oxytocin (OTR), arginine vasopressin (V1aR), dopamine (D1R, D2R) and mu-opioid (MOR). We found that social variation across individuals of the oval butterflyfish, Chaetodon lunulatus, is linked to differences in OTR,V1aR, D1R, D2R and MOR gene expression within several forebrain regions in a sexually dimorphic manner. However, this contrasted with social variation among six species representing a single evolutionary transition from pair-bonded to solitary living. Here, OTR expression within the supracommissural part of the ventral telencephalon was higher in pair-bonded than solitary species, specifically in males. These results contribute to the emerging idea that nonapeptide, dopamine and opioid signalling is a central theme to the evolution of sociality across individuals, although the precise mechanism may be flexible across sexes and species.

Multiple stressor effects on coral reef ecosystems.

Global climate change has profound implications on species distributions and ecosystem functioning. In the coastal zone, ecological responses may be driven by various biogeochemical and physical environmental factors. Synergistic interactions can occur when the combined effects of stressors exceed their individual effects. The Red Sea, characterized by strong gradients in temperature, salinity, and nutrients along the latitudinal axis provides a unique opportunity to study ecological responses over a range of these environmental variables. Using multiple linear regression models integrating in situ, satellite and oceanographic data, we investigated the response of coral reef taxa to local stressors and recent climate variability. Taxa and functional groups responded to a combination of climate (temperature, salinity, air-sea heat fluxes, irradiance, wind speed), fishing pressure and biogeochemical (chlorophyll a and nutrients - phosphate, nitrate, nitrite) factors. The regression model for each species showed interactive effects of climate, fishing pressure and nutrient variables. The nature of the effects (antagonistic or synergistic) was dependent on the species and stressor pair. Variables consistently associated with the highest number of synergistic interactions included heat flux terms, temperature, and wind speed followed by fishing pressure. Hard corals and coralline algae abundance were sensitive to changing environmental conditions where synergistic interactions decreased their percentage cover. These synergistic interactions suggest that the negative effects of fishing pressure and eutrophication may exacerbate the impact of climate change on corals. A high number of interactions were also recorded for algae, however for this group, synergistic interactions increased algal abundance. This study is unique in applying regression analysis to multiple environmental variables simultaneously to understand stressor interactions in the field. The observed responses have important implications for understanding climate change impacts on marine ecosystems and whether managing local stressors, such as nutrient enrichment and fishing activities, may help mitigate global drivers of change.

Diurnal foraging of a wild coral-reef fish Parapercis australis in relation to late-summer temperatures.

In situ observations of diurnal foraging behaviour of a common site-attached shallow reef mesopredator Parapercis australis during late summer, revealed that although diet composition was unaffected by seawater temperature (range 28.3-32.4°C), feeding strikes and distance moved increased with temperature up to 30.5°C, beyond which they sharply declined, indicative of currently living beyond their thermal optimum. Diel feeding strikes and distance moved were however, tightly linked to ambient temperature as it related to the population's apparent thermal optimum, peaking at times when it was approached (1230 and 1700 h) and declining up to four fold at times deviating from this. These findings suggest that although this population may be currently living beyond its thermal optimum, it copes by down regulating energetically costly foraging movement and consumption and under future oceanic temperatures, these behavioural modifications are probably insufficient to avoid deleterious effects on population viability without the aid of long-term acclimation or adaptation.

Global warming may disproportionately affect larger adults in a predatory coral reef fish.

Global warming is expected to reduce body sizes of ectothermic animals. Although the underlying mechanisms of size reductions remain poorly understood, effects appear stronger at latitudinal extremes (poles and tropics) and in aquatic rather than terrestrial systems. To shed light on this phenomenon, we examined the size dependence of critical thermal maxima (CTmax) and aerobic metabolism in a commercially important tropical reef fish, the leopard coral grouper (Plectropomus leopardus) following acclimation to current-day (28.5 °C) vs. projected end-of-century (33 °C) summer temperatures for the northern Great Barrier Reef (GBR). CTmax declined from 38.3 to 37.5 °C with increasing body mass in adult fish (0.45-2.82 kg), indicating that larger individuals are more thermally sensitive than smaller conspecifics. This may be explained by a restricted capacity for large fish to increase mass-specific maximum metabolic rate (MMR) at 33 °C compared with 28.5 °C. Indeed, temperature influenced the relationship between metabolism and body mass (0.02-2.38 kg), whereby the scaling exponent for MMR increased from 0.74 ± 0.02 at 28.5 °C to 0.79 ± 0.01 at 33 °C, and the corresponding exponents for standard metabolic rate (SMR) were 0.75 ± 0.04 and 0.80 ± 0.03. The increase in metabolic scaling exponents at higher temperatures suggests that energy budgets may be disproportionately impacted in larger fish and contribute to reduced maximum adult size. Such climate-induced reductions in body size would have important ramifications for fisheries productivity, but are also likely to have knock-on effects for trophodynamics and functioning of ecosystems.

Morphological and ecological trait diversity reveal sensitivity of herbivorous fish assemblages to coral reef benthic conditions.

Herbivorous fishes play a critical role in the maintenance of coral reefs through grazing and cropping of various benthic algae types. Herbivorous fish assemblages are sensitive to changes in the reef environment and are often targeted by local fisheries. This can lead to a decline in ecosystem functions if key groups are reduced. The present study investigates the morphological and ecological trait diversity of herbivorous reef fish assemblages in habitats differing in relative benthic coverage: i) coral-dominated, ii) algae-dominated, and iii) an intermediate habitat. Trait diversity for conspicuous herbivorous fishes was measured using three trait diversity indices: trait richness, trait divergence, and trait evenness. These indices were derived from in situ community surveys and feeding observations, morphological assessment of feeding mechanics from locally collected specimens, and ecological information obtained from published data. Trait diversity, reflected in higher trait evenness and lower trait richness, was lower within algae-dominated habitats than coral-dominated habitats, suggesting that algae-dominated habitats may be compromised by the lack of essential functions provided by key species. These groups reduce algal biomass and may help facilitate the survival and growth of corals, which in turn can increase coral cover. Algae-habitats were dominated with species known to consume macroalgae (rabbitfish and surgeonfish), appearing to provide essential feeding and habitat resources. These species include browsers and croppers that are fundamental in reducing algal biomass and may help facilitate the survival and growth of corals, which in turn can promote reef health. However, this habitat lacked parrotfishes known to remove turf algae and sediments, an essential function for clearing benthic space for coral settlement and other key benthic invertebrates. This study identified several species with overlapping functional roles in the coral-dominated and intermediate habitats. Still, species that were not redundant showed high trait complementarity, suggesting that their removal may result in the loss of unique functions. Importantly, we show that algae-dominated habitats supported high numbers of juvenile fishes especially in species targeted by local artisanal fishers. We also showed that the loss of trait diversity is greater than the loss of species diversity through the comparison of taxonomic and trait ß-diversity, further emphasizing the importance of trait diversity analysis in understanding ecosystem health and maintenance.

Nutrient-supplying ocean currents modulate coral bleaching susceptibility.

With predictions that mass coral bleaching will occur annually within this century, conservation efforts must focus their limited resources based on an accurate understanding of the drivers of bleaching. Here, we provide spatial and temporal evidence that excess nutrients exacerbate the detrimental effects of heat stress to spark mass coral bleaching in the Red Sea. Exploiting this region's unique oceanographic regime, where nutrients and heat stress vary independently, we demonstrate that the world's third largest coral reef system historically suffered from severe mass bleaching only when exposed to both unusually high temperature and nutrients. Incorporating nutrient-supplying ocean currents and their variability into coral bleaching forecasts will be critical for effectively guiding efforts to safeguard the reefs most likely to persist in the Anthropocene.

Does color matter? Molecular and ecological divergence in four sympatric color morphs of a coral reef fish.

Non-sex-linked color polymorphism is common in animals and can be maintained in populations via balancing selection or, when under diversifying selection, can promote divergence. Despite their potential importance in ecological interactions and the evolution of biodiversity, their function and the mechanisms by which these polymorphisms are maintained are still poorly understood. Here, we combine field observations with life history and molecular data to compare four sympatric color morphs of the coral reef fish Paracirrhites forsteri (family Cirrhitidae) in the central Red Sea. Our findings verify that the color morphs are not sex-limited, inhabit the same reefs, and do not show clear signs of avoidance or aggression among them. A barcoding approach based on 1,276 bp of mitochondrial DNA could not differentiate the color morphs. However, when 36,769 SNPs were considered, we found low but significant population structure. Focusing on 1,121 F ST outliers, we recovered distinct population clusters that corresponded to shifts in allele frequencies with each color morph harboring unique alleles. Genetic divergence at these outlier loci is accompanied by differences in growth and marginal variation in microhabitat preference. Together, life history and molecular analysis suggest subtle divergence between the color morphs in this population, the causes for which remain elusive.

Translational Molecular Ecology in practice: Linking DNA-based methods to actionable marine environmental management.

Molecular-based approaches can provide timely biodiversity assessments, showing an immense potential to facilitate decision-making in marine environmental management. However, the uptake of molecular data into environmental policy remains minimal. Here, we showcase a selection of local to global scale studies applying molecular-based methodologies for environmental management at various stages of implementation. Drawing upon lessons learned from these case-studies, we provide a roadmap to facilitate applications of DNA-based methods to marine policies and to overcome the existing challenges. The main impediment identified is the need for standardized protocols to guarantee data comparison across spatial and temporal scales. Adoption of Translational Molecular Ecology - the sustained collaboration between molecular ecologists and stakeholders, will enhance consensus with regards to the objectives, methods, and outcomes of environmental management projects. Establishing a sustained dialogue among stakeholders is key to accelerating the adoption of molecular-based approaches for marine monitoring and assessment.

Conspicuous and cryptic reef fishes from a unique and economically important region in the northern Red Sea.

Al Wajh Bank in the northern Red Sea contains an extensive coral reef system that potentially supports a novel fish community. The large (1500km2) and shallow (< 40m depth) lagoon experiences greater temperature and salinity fluctuations, as well as higher turbidity, than most other Red Sea reefs. Since these conditions often influence coral community structure and introduce physiological challenges to its resident organisms, changes in reef-associated fishes are expected. We present critical baseline data on fish biodiversity and benthic composition for the Al Wajh Bank. Underwater visual census of conspicuous fishes and standardized collections of cryptobenthic fishes were combined to provide a comprehensive assessment of these fish communities. We documented 153 fish species and operational taxonomic units, including undescribed species, within 24 families on reefs largely dominated by hard coral and soft sediment (39% and 32% respectively). The families Pomacentridae and Gobiidae contributed the most towards fish diversity and abundance. Bray-Curtis dissimilarity distances among sampled sites suggest a distinctive fish community within the lagoon, and coefficients of variation for each species show high variation in their distribution across the lagoon. Species accumulation curves predict that additional sampling would document many more species throughout Al Wajh. Our findings provide the most extensive biodiversity survey of fishes from this region to date and record the condition of the reef prior to major coastal development planned to occur in the near future.

Comparison of cryptobenthic reef fish communities among microhabitats in the Red Sea.

Knowledge of community structure within an ecosystem is essential when trying to understand the function and importance of the system and when making related management decisions. Within the larger ecosystem, microhabitats play an important role by providing inhabitants with a subset of available resources. On coral reefs, cryptobenthic fishes encompass many groups and make up an important proportion of the biodiversity. However, these fishes are relatively small, exhibit extreme visual or behavioral camouflage, and, therefore, are often overlooked. We examined the differences in fish community structure between three common reef microhabitats (live hard coral, dead coral rubble, and sand) using ichthyocide stations in the central Red Sea. Using a combination of morphological and genetic (cytochrome oxidase I (COI) barcoding) techniques, we identified 326 individuals representing 73 species spread across 17 families, from fifteen 1 m2 quadrats. Fish assemblages in the three microhabitats were significantly different from each other. Rubble microhabitats yielded the highest levels of fish abundance, richness, and diversity, followed by hard coral, and then sand. The results show that benthic composition, even at a small scale, influences cryptobenthic communities. This study also provides new COI sequence data to public databases, in order to further the research of cryptobenthic fishes in the Red Sea region.

Pair bond endurance promotes cooperative food defense and inhibits conflict in coral reef butterflyfish.

Pair bonding is generally linked to monogamous mating systems, where the reproductive benefits of extended mate guarding and/or of bi-parental care are considered key adaptive functions. However, in some species, including coral reef butterflyfishes (f. Chaetodonitidae), pair bonding occurs in sexually immature and homosexual partners, and in the absence of parental care, suggesting there must be non-reproductive adaptive benefits of pair bonding. Here, we examined whether pair bonding butterflyfishes cooperate in defense of food, conferring direct benefits to one or both partners. We found that pairs of Chaetodon lunulatus and C. baronessa use contrasting cooperative strategies. In C. lunulatus, both partners mutually defend their territory, while in C. baronessa, males prioritize territory defence; conferring improvements in feeding and energy reserves in both sexes relative to solitary counterparts. We further demonstrate that partner fidelity contributes to this function by showing that re-pairing invokes intra-pair conflict and inhibits cooperatively-derived feeding benefits, and that partner endurance is required for these costs to abate. Overall, our results suggest that in butterflyfishes, pair bonding enhances cooperative defense of prey resources, ultimately benefiting both partners by improving food resource acquisition and energy reserves.

Variation in social systems within Chaetodon butterflyfishes, with special reference to pair bonding.

For many animals, affiliative relationships such as pair bonds form the foundation of society and are highly adaptive. Animal systems amenable for comparatively studying pair bonding are important for identifying underlying biological mechanisms, but mostly exist in mammals. Better establishing fish systems will enable comparison of pair bonding mechanisms across taxonomically distant lineages that may reveal general underlying mechanistic principles. We examined the utility of wild butterflyfishes (f: Chaetodontidae; g: Chaetodon) for comparatively studying pair bonding. Using stochastic character mapping, we provide the first analysis of the evolutionary history of butterflyfish sociality, revealing that pairing is ancestral, with at least seven independent transitions to gregarious grouping and solitary behavior since the late Miocene. We then formally verified social systems in six sympatric and wide-spread species representing a clade with one ancestrally reconstructed transition from paired to solitary grouping at Lizard Island, Australia. In situ observations of the size, selective affiliation and aggression, fidelity, and sex composition of social groups confirmed that Chaetodon baronessa, C. lunulatus, and C. vagabundus are predominantly pair bonding, whereas C. rainfordi, C. plebeius, and C. trifascialis are predominantly solitary. Even in the predominantly pair bonding species, C. lunulatus, a proportion of adults (15%) are solitary. Importantly, inter- and intra-specific differences in social systems do not co-vary with other previously established attributes, including parental care. Hence, the proposed butterflyfish populations are promising for inter- and intra-species comparative analyses of pair bonding and its mechanistic underpinnings. Avenues for further developing the system are proposed, including determining whether the aforementioned utility of these species applies across their geographic disruptions.

Microplastic in the gastrointestinal tract of fishes along the Saudi Arabian Red Sea coast.

This study assesses the presence of microplastic litter in the contents of the gastrointestinal tract of 26 commercial and non-commercial fish species from four difference habitats sampled along the Saudi Arabian coast of the Red Sea. A total of 178 individual were examined for microplastics. In total, 26 microplastic fragments were found. Of these, 16 being films (61.5%) and 10 being fishing thread (38.5%). FTIR analysis revealed that the most abundant polymers were polypropylene and polyethylene. Parascolosps eriomma species sampled at Jazan registered the highest number of ingested microplastic. This fish species is benthic and feeds on benthic invertebrates. Although differences in the abundance of microplastic ingestion among species were not statistically significant, a significant change was observed when the level of ingestion of microplastics particles was compared among the habitats. The higher abundance of microplastics particles may be related to the habitats of fish and the presence of microplastics debris near the seabed. The results of this study represent a first evidence that microplastic pollution represents an emerging threat to Red Sea fishes, their food web and human consumers.

Habitat Use and Spatial Variability of Hawkfishes with a Focus on Colour Polymorphism in Paracirrhites forsteri.

Identifying relationships between fishes and their environment is an integral part of understanding coral reef ecosystems. However, this information is lacking for many species, particularly in understudied and remote regions. With coral reefs continuing to face environmental pressures, insight into abundance and distribution patterns along with resource use of fish communities will aid in advancing our ecological understanding and management processes. Based on ecological surveys of hawkfish assemblages (Family: Cirrhitidae) in the Red Sea, we reveal distinct patterns in the distribution and abundance across the continental shelf, wave exposure, and with depth, particularly in the four colour morphs of Paracirrhites forsteri. Distinct patterns were observed among hawkfishes, with higher abundance of all species recorded on reefs farther from shore and on wave exposed reef zones. Cirrhitus spilotoceps was only recorded on the exposed crest, but unlike the other species, did not associate with live coral colonies. Overall, the most abundant species was P. forsteri. This species exploited a variety of habitats but showed an affinity for complex habitats provided by live and dead coral colonies. No difference in habitat use was observed among the four colour morphs, but distinct patterns were apparent in distribution and abundance with depth. This study suggests that in addition to P. forsteri exhibiting diverse colour morphologies, these various morphotypes appear to have corresponding ecological differences in the Red Sea. To better understand this, further studies are needed to identify what these differences extend to and the mechanisms involved.

Habitat Selectivity and Reliance on Live Corals for Indo-Pacific Hawkfishes (Family: Cirrhitidae).

Hawkfishes (family: Cirrhitidae) are small conspicuous reef predators that commonly perch on, or shelter within, the branches of coral colonies. This study examined habitat associations of hawkfishes, and explicitly tested whether hawkfishes associate with specific types of live coral. Live coral use and habitat selectivity of hawkfishes was explored at six locations from Chagos in the central Indian Ocean extending east to Fiji in the Pacific Ocean. A total of 529 hawkfishes from seven species were recorded across all locations with 63% of individuals observed perching on, or sheltering within, live coral colonies. Five species (all except Cirrhitus pinnulatus and Cirrhitichthys oxycephalus) associated with live coral habitats. Cirrhitichthys falco selected for species of Pocillopora while Paracirrhites arcatus and P. forsteri selected for both Pocillopora and Acropora, revealing that these habitats are used disproportionately more than expected based on the local cover of these coral genera. Habitat selection was consistent across geographic locations, and species of Pocillopora were the most frequently used and most consistently selected even though this coral genus never comprised more than 6% of the total coral cover at any of the locations. Across locations, Paracirrhites arcatus and P. forsteri were the most abundant species and variation in their abundance corresponded with local patterns of live coral cover and abundance of Pocilloporid corals, respectively. These findings demonstrate the link between small predatory fishes and live coral habitats adding to the growing body of literature highlighting that live corals (especially erect branching corals) are critically important for sustaining high abundance and diversity of fishes on coral reefs.

Specialization in habitat use by coral reef damselfishes and their susceptibility to habitat loss.

While it is generally assumed that specialist species are more vulnerable to disturbance compared with generalist counterparts, this has rarely been tested in coastal marine ecosystems, which are increasingly subject to a wide range of natural and anthropogenic disturbances. Habitat specialists are expected to be more vulnerable to habitat loss because habitat availability exerts a greater limitation on population size, but it is also possible that specialist species may escape effects of disturbance if they use habitats that are generally resilient to disturbance. This study quantified specificity in use of different coral species by six coral-dwelling damselfishes (Chromis viridis, C. atripectoralis, Dascyllus aruanus, D. reticulatus, Pomacentrus moluccensis, and P. amboinensis) and related habitat specialization to proportional declines in their abundance following habitat degradation caused by outbreaks of the coral eating starfish, Acanthaster planci. The coral species preferred by most coral-dwelling damselfishes (e.g., Pocillopora damicornis) were frequently consumed by coral eating crown-of-thorns starfish, such that highly specialized damselfishes were disproportionately affected by coral depletion, despite using a narrower range of different coral species. Vulnerability of damselfishes to this disturbance was strongly correlated with both their reliance on corals and their degree of habitat specialization. Ongoing disturbances to coral reef ecosystems are expected, therefore, to lead to fundamental shifts in the community structure of fish communities where generalists are favored over highly specialist species.