Seabirds boost coral reef resilience.

Global climate change threatens tropical coral reefs, yet local management can influence resilience. While increasing anthropogenic nutrients reduce coral resistance and recovery, it is unknown how the loss, or restoration, of natural nutrient flows affects reef recovery. Here, we test how natural seabird-derived nutrient subsidies, which are threatened by invasive rats, influence the mechanisms and patterns of reef recovery following an extreme marine heatwave using multiyear field experiments, repeated surveys, and Bayesian modeling. Corals transplanted from rat to seabird islands quickly assimilated seabird-derived nutrients, fully acclimating to new nutrient conditions within 3 years. Increased seabird-derived nutrients, in turn, caused a doubling of coral growth rates both within individuals and across entire reefs. Seabirds were also associated with faster recovery time of Acropora coral cover (<4 years) and more dynamic recovery trajectories of entire benthic communities. We conclude that restoring seabird populations and associated nutrient pathways may foster greater coral reef resilience through enhanced growth and recovery rates of corals.

Sustainable reference points for multispecies coral reef fisheries.

Sustainably managing fisheries requires regular and reliable evaluation of stock status. However, most multispecies reef fisheries around the globe tend to lack research and monitoring capacity, preventing the estimation of sustainable reference points against which stocks can be assessed. Here, combining fish biomass data for >2000 coral reefs, we estimate site-specific sustainable reference points for coral reef fisheries and use these and available catch estimates to assess the status of global coral reef fish stocks. We reveal that >50% of sites and jurisdictions with available information have stocks of conservation concern, having failed at least one fisheries sustainability benchmark. We quantify the trade-offs between biodiversity, fish length, and ecosystem functions relative to key benchmarks and highlight the ecological benefits of increasing sustainability. Our approach yields multispecies sustainable reference points for coral reef fisheries using environmental conditions, a promising means for enhancing the sustainability of the world's coral reef fisheries.

Research priorities for the sustainability of coral-rich western Pacific seascapes.

Nearly a billion people depend on tropical seascapes. The need to ensure sustainable use of these vital areas is recognised, as one of 17 policy commitments made by world leaders, in Sustainable Development Goal (SDG) 14 ('Life below Water') of the United Nations. SDG 14 seeks to secure marine sustainability by 2030. In a time of increasing social-ecological unpredictability and risk, scientists and policymakers working towards SDG 14 in the Asia-Pacific region need to know: (1) How are seascapes changing? (2) What can global society do about these changes? and (3) How can science and society together achieve sustainable seascape futures? Through a horizon scan, we identified nine emerging research priorities that clarify potential research contributions to marine sustainability in locations with high coral reef abundance. They include research on seascape geological and biological evolution and adaptation; elucidating drivers and mechanisms of change; understanding how seascape functions and services are produced, and how people depend on them; costs, benefits, and trade-offs to people in changing seascapes; improving seascape technologies and practices; learning to govern and manage seascapes for all; sustainable use, justice, and human well-being; bridging communities and epistemologies for innovative, equitable, and scale-crossing solutions; and informing resilient seascape futures through modelling and synthesis. Researchers can contribute to the sustainability of tropical seascapes by co-developing transdisciplinary understandings of people and ecosystems, emphasising the importance of equity and justice, and improving knowledge of key cross-scale and cross-level processes, feedbacks, and thresholds.

Macroalgae exhibit diverse responses to human disturbances on coral reefs.

Scientists and managers rely on indicator taxa such as coral and macroalgal cover to evaluate the effects of human disturbance on coral reefs, often assuming a universally positive relationship between local human disturbance and macroalgae. Despite evidence that macroalgae respond to local stressors in diverse ways, there have been few efforts to evaluate relationships between specific macroalgae taxa and local human-driven disturbance. Using genus-level monitoring data from 1205 sites in the Indian and Pacific Oceans, we assess whether macroalgae percent cover correlates with local human disturbance while accounting for factors that could obscure or confound relationships. Assessing macroalgae at genus level revealed that no genera were positively correlated with all human disturbance metrics. Instead, we found relationships between the division or genera of algae and specific human disturbances that were not detectable when pooling taxa into a single functional category, which is common to many analyses. The convention to use percent cover of macroalgae as an indication of local human disturbance therefore likely obscures signatures of local anthropogenic threats to reefs. Our limited understanding of relationships between human disturbance, macroalgae taxa, and their responses to human disturbances impedes the ability to diagnose and respond appropriately to these threats.

On the Challenges of Identifying Benthic Dominance on Anthropocene Coral Reefs.

The concept of dominance is frequently used to describe changes in rapidly reconfiguring ecosystems, but the definition of dominance can vary widely among studies. Using coral reefs as a model, we use extensive benthic composition data to explore how variability in applying dominance concepts can shape perceptions. We reveal that coral dominance is sensitive to the exclusion of key algal groups and the categorization of other benthic groups, with ramifications for detecting an ecosystem phase shift. For example, ignoring algal turf inflates the dominance of hard and soft corals in the benthic habitats underpinning reef ecosystems. We need a consensus on how dominance concepts are applied so that we can build a more comprehensive understanding of ecosystem shifts across a broad range of aquatic and terrestrial settings. For reefs, we highlight the benefits of comprehensive and inclusive surveys for evaluating and managing the altered ecosystem states that are emerging in the Anthropocene.

Seabird diversity and biomass enhance cross-ecosystem nutrient subsidies.

Mobile consumers are key vectors of cross-ecosystem nutrients, yet have experienced population declines which threaten their ability to fill this role. Despite their importance and vulnerability, there is little information on how consumer biodiversity, in addition to biomass, influences the magnitude of nutrient subsidies. Here, we show that both biomass and diversity of seabirds enhanced the provisioning of nutrients across tropical islands and coral reefs, but their relative influence varied across systems. Seabird biomass was particularly important for terrestrial and near-shore subsidies and enhancing fish biomass, while seabird diversity was associated with nutrient subsidies further offshore. The positive effects of diversity were likely driven by high functional complementarity among seabird species in traits related to nutrient storage and provisioning. However, introduced rats and non-native vegetation reduced seabird biomass and diversity, with rats having a stronger effect on biomass and vegetation having a stronger effect on diversity. Accordingly, the restoration of cross-ecosystem nutrient flows provided by seabirds will likely be most successful when both stressors are removed, thus protecting both high biomass and diversity. Recognizing the importance of mobile consumer diversity and biomass, and their underlying drivers, is a necessary step to conserving these species and the ecosystem functions they provide.

Tropical larval and juvenile fish critical swimming speed (U-crit) and morphology data.

Fish swimming capacity is a key life history trait critical to many aspects of their ecology. U-crit (critical) swimming speeds provide a robust, repeatable relative measure of swimming speed that can serve as a useful surrogate for other measures of swimming performance. Here we collate and make available one the most comprehensive datasets on U-crit swimming abilities of tropical marine fish larvae and pelagic juveniles, most of which are reef associated as adults. The dataset includes U-crit speed measurements for settlement stage fishes across a large range of species and families obtained mostly from field specimens collected in light traps and crest nets; and the development of swimming abilities throughout ontogeny for a range of species using reared larvae. In nearly all instances, the size of the individual was available, and in many cases, data include other morphological measurements (e.g. "propulsive area") useful for predicting swimming capacity. We hope these data prove useful for further studies of larval swimming performance and other broader syntheses.

Climate-induced increases in micronutrient availability for coral reef fisheries.

Climate change is transforming coral reefs, threatening supply of essential dietary micronutrients from small-scale fisheries to tropical coastal communities. Yet the nutritional value of reef fisheries and climate impacts on micronutrient availability remain unclear, hindering efforts to sustain food and nutrition security. Here, we measure nutrient content in coral reef fishes in Seychelles and show that reef fish are important sources of selenium and zinc and contain levels of calcium, iron, and omega-3 fatty acids comparable with other animal-source foods. Using experimental fishing, we demonstrate that iron and zinc are enriched in fishes caught on regime-shifted macroalgal habitats, whereas selenium and omega-3 varied among species. We find substantial increases in nutrients available to fisheries over two decades following coral bleaching, particularly for iron and zinc after macroalgal regime shifts. Our findings indicate that, if managed sustainably, coral reef fisheries could remain important micronutrient sources along tropical coastlines despite escalating climate impacts.

Precision and cost-effectiveness of bioindicators to estimate nutrient regimes on coral reefs.

Bioindicators are useful for determining nutrient regimes in marine environments, but their ability to evaluate corals reefs in different ecological states is poorly understood. The precision, availability and congruency of eight potential bioindicators (brown macroalgae, green macroalgae, turf algae, cyanobacteria, soft corals, zoanthids, sponges, and sediment) and their stable isotopic and elemental signatures (δ15N, δ13C, %N, %C, and C:N Ratio) were assessed across 21 reefs in the Inner Seychelles. The coefficient of variation (CoV) for δ15N showed that green and brown macroalgae were highly precise (2.47 ± 0.95, n = 11; 4.68 ± 1.33, n = 16, respectively), though were less common on coral-mortality reefs relative to macroalgal-dominated ones. Zoanthids were also highly precise for δ15N (2.98 ± 1.20), but were more readily available regardless of reef state (n = 18). Congruency was low among these indicators, suggesting that different physiological mechanisms for nutrient processing have a stronger influence on a bioindicator's effectiveness than reef state.

Coral larval recruitment in north-western Australia predicted by regional and local conditions.

Understanding ecological processes that shape contemporary and future communities facilitates knowledge-based environmental management. In marine ecosystems, one of the most important processes is the supply of new recruits into a population. Here, we investigated spatiotemporal variability in coral recruitment at 15 reefs throughout the Dampier Archipelago, north-western Australia between 2015 and 2017 and identified the best environmental predictors for coral recruitment patterns over this period. Large differences in recruitment were observed among years with the average density of recruits increasing by 375% from 0.017 recruits cm-2 in 2015 to 0.059 recruits cm-2 in 2017. Despite differences in recruitment among years, the rank order of coral recruit density among reefs remained similar among years, suggesting that spatial variation in recruitment within the Dampier Archipelago is partly deterministic and predictable. The density of coral recruits was best explained by percent cover of live corals at both local (within 5 m) and meso-scales (within 15 km), water turbidity and an oceanographic model that predicted larval dispersal. The highest density of coral recruits (~0.13 recruits cm-2 or 37 recruits per tile) occurred on reefs within sub-regions (15 km) with greater than 35% coral cover, low to moderate turbidity (KD490 < 0.2) and moderate to high modelled predictions of larval dispersal. Our results demonstrate that broad-scale larval dispersal models, when combined with local metrics of percent hard coral cover and water turbidity, can reliably predict the relative abundance of coral recruits over large geographical areas and thus can identify hotspots of recruit abundance and potential recovery following environmental disturbances; information that is essential for effective management of coral reefs.

Knowledge Gaps in the Biology, Ecology, and Management of the Pacific Crown-of-Thorns Sea Star Acanthaster sp. on Australia's Great Barrier Reef.

AbstractCrown-of-thorns sea stars (Acanthaster sp.) are among the most studied coral reef organisms, owing to their propensity to undergo major population irruptions, which contribute to significant coral loss and reef degradation throughout the Indo-Pacific. However, there are still important knowledge gaps pertaining to the biology, ecology, and management of Acanthaster sp. Renewed efforts to advance understanding and management of Pacific crown-of-thorns sea stars (Acanthaster sp.) on Australia's Great Barrier Reef require explicit consideration of relevant and tractable knowledge gaps. Drawing on established horizon scanning methodologies, this study identified contemporary knowledge gaps by asking active and/or established crown-of-thorns sea star researchers to pose critical research questions that they believe should be addressed to improve the understanding and management of crown-of-thorns sea stars on the Great Barrier Reef. A total of 38 participants proposed 246 independent research questions, organized into 7 themes: feeding ecology, demography, distribution and abundance, predation, settlement, management, and environmental change. Questions were further assigned to 48 specific topics nested within the 7 themes. During this process, redundant questions were removed, which reduced the total number of distinct research questions to 172. Research questions posed were mostly related to themes of demography (46 questions) and management (48 questions). The dominant topics, meanwhile, were the incidence of population irruptions (16 questions), feeding ecology of larval sea stars (15 questions), effects of elevated water temperature on crown-of-thorns sea stars (13 questions), and predation on juveniles (12 questions). While the breadth of questions suggests that there is considerable research needed to improve understanding and management of crown-of-thorns sea stars on the Great Barrier Reef, the predominance of certain themes and topics suggests a major focus for new research while also providing a roadmap to guide future research efforts.

Size-specific recolonization success by coral-dwelling damselfishes moderates resilience to habitat loss.

Increasing degradation of coral reef ecosystems and specifically, loss of corals is causing significant and widespread declines in the abundance of coral reef fishes, but the proximate cause(s) of these declines are largely unknown. Here, we examine specific responses to host coral mortality for three species of coral-dwelling damselfishes (Dascyllus aruanus, D. reticulatus, and Pomacentrus moluccensis), explicitly testing whether these fishes can successfully move and recolonize nearby coral hosts. Responses of fishes to localized coral loss was studied during population irruptions of coral feeding crown-of-thorns starfish, where starfish consumed 29 (34%) out of 85 coral colonies, of which 25 (86%) were occupied by coral-dwelling damselfishes. Damselfishes were not tagged or individually recognizable, but changes in the colonization of different coral hosts was assessed by carefully assessing the number and size of fishes on every available coral colony. Most damselfishes (> 90%) vacated dead coral hosts within 5 days, and either disappeared entirely (presumed dead) or relocated to nearby coral hosts. Displaced fishes only ever colonized corals already occupied by other coral-dwelling damselfishes (mostly conspecifics) and colonization success was strongly size-dependent. Despite movement of damselfishes to surviving corals, the local abundance of coral-dependent damselfishes declined in approximate accordance with the proportional loss of coral habitat. These results suggest that even if alternative coral hosts are locally abundant, there are significant biological constraints on movement of coral-dwelling damselfishes and recolonization of alternative coral habitats, such that localized persistence of habitat patches during moderate or patchy disturbances do not necessarily provide resilience against overall habitat loss.

Zone specific trends in coral cover, genera and growth-forms in the World-Heritage listed Ningaloo Reef.

On coral reefs, changes in the cover and relative abundance of hard coral taxa often follow disturbance. Although the ecological responses of common coral taxa have been well documented, little is known about the ecological responses of uncommon coral taxa or of coral morphological groups across multiple adjacent reef zones. We used Multivariate Auto-Regressive State-Space modelling to assess the rate and direction of change of hard coral cover across a variety of coral genera, growth forms, and susceptibility to bleaching and physical damage covering multiple reef zones at northern Ningaloo Reef in Western Australia. Trends were assessed between 2007 and 2016, during which multiple episodic disturbances occurred including cyclones and a heatwave. We provide evidence of zone specific trends, not only in total hard coral cover, but also in taxonomic and morphological groups of corals at Ningaloo Reef. Declines in total coral cover on the reef flat corresponded with declines in fast growing corals, particularly Acropora. In contrast, total coral cover on the reef slope and inshore (lagoon) did not undergo significant change, despite divergent trajectories of individual genera. Importantly, we also show that changes in the composition of coral assemblages can be detected using a morphological based approach when changes are not evident using a taxonomic approach. Therefore, we recommend that future assessments of coral reef trends incorporate not just standard metrics such as total coral cover, but also metrics that provide for detailed descriptions of trends in common and uncommon taxa and morphological groups across multiple reef zones.

Early recovery dynamics of turbid coral reefs after recurring bleaching events.

The worlds' coral reefs are declining due to the combined effects of natural disturbances and anthropogenic pressures including thermal coral bleaching associated with global climate change. Nearshore corals are receiving increased anthropogenic stress from coastal development and nutrient run-off. Considering forecast increases in global temperatures, greater understanding of drivers of recovery on nearshore coral reefs following widespread bleaching events is required to inform management of local stressors. The west Pilbara coral reefs, with cross-shelf turbidity gradients coupled with a large nearby dredging program and recent history of repeated coral bleaching due to heat stress, represent an opportune location to study recovery from multiple disturbances. Mean coral cover at west Pilbara reefs was monitored from 2009 to 2018 and declined from 45% in 2009 to 5% in 2014 following three heat waves. Recruitment and juvenile abundance of corals were monitored from 2014 to 2018 and were combined with biological and physical data to identify which variables enhanced or hindered early-stage coral recovery of all hard corals and separately for the acroporids, the genera principally responsible for recovery in the short-term (<7 years). From 2014 to 2018, coral cover increased from 5 to 10% but recovery varied widely among sites (0-13%). Hard coral cover typically recovered most at shallower sites that had higher abundance of herbivorous fish, less macroalgae, and lower turbidity. Similarly, acroporid corals recovered most at sites with lower turbidity and macroalgal cover. Juvenile acroporid densities were a good indicator of recovery at least two years after they were recorded. However, recruitment to settlement tiles was not a good predictor of total coral or acroporid recovery. This study shows that coral recovery can be slower in areas of high turbidity and the rate may be reduced by local pressures, such as dredging. Management should focus on improving or maintaining local water quality to increase the likelihood of coral recovery under climate stress. Further, in turbid environments, juvenile coral density predicts early coral recovery better than recruits on tiles and may be a more cost-effective technique for monitoring recovery potential.

Biodiversity increases ecosystem functions despite multiple stressors on coral reefs.

Positive relationships between biodiversity and ecosystem functioning (BEF) highlight the importance of conserving biodiversity to maintain key ecosystem functions and associated services. Although natural systems are rapidly losing biodiversity due to numerous human-caused stressors, our understanding of how multiple stressors influence BEF relationships comes largely from small, experimental studies. Here, using remote assemblages of coral reef fishes, we demonstrate strong, non-saturating relationships of biodiversity with two ecosystem functions: biomass and productivity. These positive relationships were robust both to an extreme heatwave that triggered coral bleaching and to invasive rats which disrupt nutrient subsidies from native seabirds. Despite having only minor effects on BEF relationships, both stressors still decreased ecosystem functioning via other pathways. The extreme heatwave reduced biodiversity, which, due to the strong BEF relationships, ultimately diminished both ecosystem functions. Conversely, the loss of cross-system nutrient subsidies directly decreased biomass. These results demonstrate multiple ways by which human-caused stressors can reduce ecosystem functioning, despite robust BEF relationships, in natural high-diversity assemblages.

Meeting fisheries, ecosystem function, and biodiversity goals in a human-dominated world.

The worldwide decline of coral reefs necessitates targeting management solutions that can sustain reefs and the livelihoods of the people who depend on them. However, little is known about the context in which different reef management tools can help to achieve multiple social and ecological goals. Because of nonlinearities in the likelihood of achieving combined fisheries, ecological function, and biodiversity goals along a gradient of human pressure, relatively small changes in the context in which management is implemented could have substantial impacts on whether these goals are likely to be met. Critically, management can provide substantial conservation benefits to most reefs for fisheries and ecological function, but not biodiversity goals, given their degraded state and the levels of human pressure they face.

Changing role of coral reef marine reserves in a warming climate.

Coral reef ecosystems are among the first to fundamentally change in structure due to climate change, which leads to questioning of whether decades of knowledge regarding reef management is still applicable. Here we assess ecological responses to no-take marine reserves over two decades, spanning a major climate-driven coral bleaching event. Pre-bleaching reserve responses were consistent with a large literature, with higher coral cover, more species of fish, and greater fish biomass, particularly of upper trophic levels. However, in the 16 years following coral mortality, reserve effects were absent for the reef benthos, and greatly diminished for fish species richness. Positive fish biomass effects persisted, but the groups of fish benefiting from marine reserves profoundly changed, with low trophic level herbivores dominating the responses. These findings highlight that while marine reserves still have important roles on coral reefs in the face of climate change, the species and functional groups they benefit will be substantially altered.

Thermal stress induces persistently altered coral reef fish assemblages.

Ecological communities are reorganizing in response to warming temperatures. For continuous ocean habitats this reorganization is characterized by large-scale species redistribution, but for tropical discontinuous habitats such as coral reefs, spatial isolation coupled with strong habitat dependence of fish species imply that turnover and local extinctions are more significant mechanisms. In these systems, transient marine heatwaves are causing coral bleaching and profoundly altering habitat structure, yet despite severe bleaching events becoming more frequent and projections indicating annual severe bleaching by the 2050s at most reefs, long-term effects on the diversity and structure of fish assemblages remain unclear. Using a 23-year time series spanning a thermal stress event, we describe and model structural changes and recovery trajectories of fish communities after mass bleaching. Communities changed fundamentally, with the new emergent communities dominated by herbivores and persisting for >15 years, a period exceeding realized and projected intervals between thermal stress events on coral reefs. Reefs which shifted to macroalgal states had the lowest species richness and highest compositional dissimilarity, whereas reefs where live coral recovered exceeded prebleaching fish richness, but remained dissimilar to prebleaching compositions. Given realized and projected frequencies of bleaching events, our results show that fish communities historically associated with coral reefs will not re-establish, requiring substantial adaptation by managers and resource users.

Seabird nutrient subsidies alter patterns of algal abundance and fish biomass on coral reefs following a bleaching event.

Cross-ecosystem nutrient subsidies play a key role in the structure and dynamics of recipient communities, but human activities are disrupting these links. Because nutrient subsidies may also enhance community stability, the effects of losing these inputs may be exacerbated in the face of increasing climate-related disturbances. Nutrients from seabirds nesting on oceanic islands enhance the productivity and functioning of adjacent coral reefs, but it is unknown whether these subsidies affect the response of coral reefs to mass bleaching events or whether the benefits of these nutrients persist following bleaching. To answer these questions, we surveyed benthic organisms and fishes around islands with seabirds and nearby islands without seabirds due to the presence of invasive rats. Surveys were conducted in the Chagos Archipelago, Indian Ocean, immediately before the 2015-2016 mass bleaching event and, in 2018, two years following the bleaching event. Regardless of the presence of seabirds, relative coral cover declined by 32%. However, there was a post-bleaching shift in benthic community structure around islands with seabirds, which did not occur around islands with invasive rats, characterized by increases in two types of calcareous algae (crustose coralline algae [CCA] and Halimeda spp.). All feeding groups of fishes were positively affected by seabirds, but only herbivores and piscivores were unaffected by the bleaching event and sustained the greatest difference in biomass between islands with seabirds versus those with invasive rats. By contrast, corallivores and planktivores, both of which are coral-dependent, experienced the greatest losses following bleaching. Even though seabird nutrients did not enhance community-wide resistance to bleaching, they may still promote recovery of these reefs through their positive influence on CCA and herbivorous fishes. More broadly, the maintenance of nutrient subsidies, via strategies including eradication of invasive predators, may be important in shaping the response of ecological communities to global climate change.

Trait structure and redundancy determine sensitivity to disturbance in marine fish communities.

Trait diversity is believed to influence ecosystem dynamics through links between organismal traits and ecosystem processes. Theory predicts that key traits and high trait redundancy-large species richness and abundance supporting the same traits-can buffer communities against environmental disturbances. While experiments and data from simple ecological systems lend support, large-scale evidence from diverse, natural systems under major disturbance is lacking. Here, using long-term data from both temperate (English Channel) and tropical (Seychelles Islands) fishes, we show that sensitivity to disturbance depends on communities' initial trait structure and initial trait redundancy. In both ecosystems, we found that increasing dominance by climatically vulnerable traits (e.g., small, fast-growing pelagics/corallivores) rendered fish communities more sensitive to environmental change, while communities with higher trait redundancy were more resistant. To our knowledge, this is the first study demonstrating the influence of trait structure and redundancy on community sensitivity over large temporal and spatial scales in natural systems. Our results exemplify a consistent link between biological structure and community sensitivity that may be transferable across ecosystems and taxa and could help anticipate future disturbance impacts on biodiversity and ecosystem functioning.