Evidence for managing herbivores for reef resilience.

Herbivore management is an important tool for resilience-based approaches to coral reef conservation, and evidence-based science is needed to enact successful management. We synthesized data from multiple monitoring programs in Hawai'i to measure herbivore biomass and benthic condition over a 10-year period preceding any major coral bleaching. We analysed data from 20 242 transects alongside data on 27 biophysical and human drivers and found herbivore biomass was highly variable throughout Hawai'i, with high values in remote locations and the lowest values near population centres. Both human and biophysical drivers explained variation in herbivore biomass, and among the human drivers both fishing and land-based pollution had negative effects on biomass. We also found evidence that herbivore functional group biomass is strongly linked to benthic condition, and that benthic condition is sensitive to changes in herbivore biomass associated with fishing. We show that when herbivore biomass is below 80% of potential biomass, benthic condition is predicted to decline. We also show that a range of management actions, including area-specific fisheries regulations and gear restrictions, can increase parrotfish biomass. Together, these results provide lines of evidence to support managing herbivores as an effective strategy for maintaining or bolstering reef resilience in a changing climate.

Decreased tourism during the COVID-19 pandemic positively affects reef fish in a high use marine protected area.

Humans alter ecosystems through both consumptive and non-consumptive effects. Consumptive effects occur through hunting, fishing and collecting, while non-consumptive effects occur due to the responses of wildlife to human presence. While marine conservation efforts have focused on reducing consumptive effects, managing human presence is also necessary to maintain and restore healthy ecosystems. Area closures and the tourism freeze related to the COVID-19 pandemic provided a unique natural experiment to measure the effects of decreased tourism on fish behavior in a high use no-take marine protected area (MPA) in Hawai`i. We found that when tourism shut down due to COVID restrictions in 2020, fish biomass increased and predatory species increased usage of shallow habitats, where tourists typically concentrate. When tourism resumed, fish biomass and habitat use returned to pre-pandemic levels. These displacement effects change fish community composition and biomass, which could affect key processes such as spawning, foraging and resting, and have knock-on effects that compromise ecosystem function and resilience. Managing non-consumptive uses, especially in heavily-visited MPAs, should be considered for sustainability of these ecosystems.

Climate-assisted persistence of tropical fish vagrants in temperate marine ecosystems.

Rising temperatures and extreme climate events are propelling tropical species into temperate marine ecosystems, but not all species can persist. Here, we used the heatwave-driven expatriation of tropical Black Rabbitfish (Siganus fuscescens) to the temperate environments of Western Australia to assess the ecological and evolutionary mechanisms that may entail their persistence. Population genomic assays for this rabbitfish indicated little genetic differentiation between tropical residents and vagrants to temperate environments due to high migration rates, which were likely enhanced by the marine heatwave. DNA metabarcoding revealed a diverse diet for this species based on phytoplankton and algae, as well as an ability to feed on regional resources, including kelp. Irrespective of future climate scenarios, these macroalgae-consuming vagrants may self-recruit in temperate environments and further expand their geographic range by the year 2100. This expansion may compromise the health of the kelp forests that form Australia's Great Southern Reef. Overall, our study demonstrates that projected favourable climate conditions, continued large-scale genetic connectivity between populations, and diet versatility are key for tropical range-shifting fish to establish in temperate ecosystems.

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.

Using species connectivity to achieve coordinated large-scale marine conservation efforts in the Red Sea.

In the face of increasing anthropogenic threats, coastal nations need to reach common ground for effective marine conservation. Understanding species' connectivity can reveal how nations share resources, demonstrating the need for cooperative protection efforts. Unfortunately, connectivity information is rarely integrated into the design of marine protected areas (MPAs). This is exemplified in the Red Sea where biodiversity is only nominally protected by a non-cohesive network of small-sized MPAs, most of which are barely implemented. Here, we showcase the potential of using connectivity patterns of flagship species to consolidate conservation efforts in the Red Sea. We argue that a large-scale MPA (LSMPA) would more effectively preserve Red Sea species' multinational migration routes. A connectivity-informed LSMPA approach provides thus one avenue to unite coastal nations toward acting for the common good of conservation and reverse the global decline in marine biodiversity.

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.

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.

Acclimatization of massive reef-building corals to consecutive heatwaves.

Reef-building corals typically live close to the upper limits of their thermal tolerance and even small increases in summer water temperatures can lead to bleaching and mortality. Projections of coral reef futures based on forecasts of ocean temperatures indicate that by the end of this century, corals will experience their current thermal thresholds annually, which would lead to the widespread devastation of coral reef ecosystems. Here, we use skeletal cores of long-lived Porites corals collected from 14 reefs across the northern Great Barrier Reef, the Coral Sea, and New Caledonia to evaluate changes in their sensitivity to heat stress since 1815. High-density 'stress bands'-indicative of past bleaching-first appear during a strong pre-industrial El Niño event in 1877 but become significantly more frequent in the late twentieth and early twenty-first centuries in accordance with rising temperatures from anthropogenic global warming. However, the proportion of cores with stress bands declines following successive bleaching events in the twenty-first century despite increasing exposure to heat stress. Our findings demonstrate an increase in the thermal tolerance of reef-building corals and offer a glimmer of hope that at least some coral species can acclimatize fast enough to keep pace with global warming.

Investigating marine bio-calcification mechanisms in a changing ocean with in vivo and high-resolution ex vivo Raman spectroscopy.

Ocean acidification poses a serious threat to marine calcifying organisms, yet experimental and field studies have found highly diverse responses among species and environments. Our understanding of the underlying drivers of differential responses to ocean acidification is currently limited by difficulties in directly observing and quantifying the mechanisms of bio-calcification. Here, we present Raman spectroscopy techniques for characterizing the skeletal mineralogy and calcifying fluid chemistry of marine calcifying organisms such as corals, coralline algae, foraminifera, and fish (carbonate otoliths). First, our in vivo Raman technique is the ideal tool for investigating non-classical mineralization pathways. This includes calcification by amorphous particle attachment, which has recently been controversially suggested as a mechanism by which corals resist the negative effects of ocean acidification. Second, high-resolution ex vivo Raman mapping reveals complex banding structures in the mineralogy of marine calcifiers, and provides a tool to quantify calcification responses to environmental variability on various timescales from days to years. We describe the new insights into marine bio-calcification that our techniques have already uncovered, and we consider the wide range of questions regarding calcifier responses to global change that can now be proposed and addressed with these new Raman spectroscopy tools.

Diversification and functional evolution of reef fish feeding guilds.

A core eco-evolutionary aim is to better understand the factors driving the diversification of functions in ecosystems. Using phylogenetic, trophic, and functional information, we tested whether trophic habits (i.e. feeding guilds) affect lineage and functional diversification in two major radiations of reef fishes. Our results from wrasses (Labridae) and damselfishes (Pomacentridae) do not fully support the 'dead-end' hypothesis that specialisation leads to reduce speciation rates because the tempo of lineage diversification did not substantially vary among guilds in both fish families. Our findings also demonstrate a tight relationship between trophic habits and functional roles held by fish in reef ecosystems, which is not associated with a variation in the tempo of functional diversification among guilds. By illustrating the pivotal importance of the generalist feeding strategy during the evolutionary history of reef fishes, our study emphasises the role of this feeding guild as a reservoir for future diversity.

Genetic diversity mirrors trophic ecology in coral reef fish feeding guilds.

Genetic diversity is essential for species persistence because it provides the raw material for evolution. For marine organisms, short pelagic larval duration (PLD) and small population size are characteristics generally assumed to associate with low genetic diversity. The ecological diversity of organisms may also affect genetic diversity with an expected corollary that more restricted habitat and dietary requirements could lead to a reduced genetic diversity because of pronounced genetic structuring. Here, we tested whether groups of species with narrower trophic niches displayed lower genetic diversity than those with broader niches. In order to test those predictions, we used different trophic guilds (i.e., groups of species having similar trophic habits) of coral reef damselfishes in Moorea (French Polynesia) for which we determined their genetic diversity using restriction site-associated DNA sequencing (RADseq) and their trophic ecology with stomach contents and stable isotope data. We found that pelagic feeders- the guild picking zooplankton in the water column- exhibited the lowest genetic diversity despite having the longest PLD and the largest population size. This guild had also the lowest variation in habitat characteristics and dietary composition compared to benthic feeders (i.e., those mainly grazing on algae) and the intermediate group (i.e., those feeding on zooplankton, filamentous algae and small benthic invertebrates). Our findings highlight the association between trophic ecology and genetic diversity that should be more commonly investigated in population genetics.