Coral reef ecosystems are being fundamentally restructured by local human impacts and climate-driven marine heatwaves that trigger mass coral bleaching and mortality(1). Reducing local impacts can increase reef resistance to and recovery from bleaching(2). However, resource managers lack clear advice on targeted actions that best support coral reefs under climate change(3) and sector-based governance means most land- and sea-based management efforts remain siloed(4). Here we combine surveys of reef change with a unique 20-year time series of land-sea human impacts that encompassed an unprecedented marine heatwave in Hawai'i. Reefs with increased herbivorous fish populations and reduced land-based impacts, such as wastewater pollution and urban runoff, had positive coral cover trajectories predisturbance. These reefs also experienced a modest reduction in coral mortality following severe heat stress compared to reefs with reduced fish populations and enhanced land-based impacts. Scenario modelling indicated that simultaneously reducing land-sea human impacts results in a three- to sixfold greater probability of a reef having high reef-builder cover four years postdisturbance than if either occurred in isolation. International efforts to protect 30% of Earth's land and ocean ecosystems by 2030 are underway(5). Our results reveal that integrated land-sea management could help achieve coastal ocean conservation goals and provide coral reefs with the best opportunity to persist in our changing climate.
Abstract Coastal ecosystems are disproportionally inhabited by global human population. Consequently, human impacts originating from land and sea combine with climate-driven disturbances to fundamentally restructure nearshore marine ecosystems. These coincident human stressors are especially acute in the tropics where population centres concentrate along shorelines and marine heatwaves increasingly trigger mass coral bleaching and mortality. However, despite decades of research, we lack consensus as to whether local management supports coral reef resilience under climate change. Here we combined recurring reef surveys with a unique time series of land-sea human impacts over a 20-year period that encompassed an unprecedented marine heatwave in Hawaiʻi. Reefs with high fish biomass and reduced land-based impacts such as wastewater pollution had positive coral trajectories pre-disturbance and experienced minimal coral loss following severe heat stress. Concurrent land-sea management resulted in a 3- to 7-fold increase in the probability of a reef having high reef-builder cover four years post-disturbance. International efforts to conserve 30% of Earth’s ecosystems are gaining momentum, but do not intrinsically link land and ocean conservation targets. Our findings suggest coupled land-sea policy measures are required to realise global conservation goals and provide coral reefs with the best opportunity for persistence in our changing climate.
Approximately one-third of long rivers remain free-flowing, and rivers face a range of ongoing and future threats. In response, there is a heightened call for actions to reverse the freshwater biodiversity crisis, including through formal global targets for protection. The Aichi Biodiversity Targets called for the protection of 17% of inland water areas by 2020. Here, we examine the levels and spatial patterns of protection for a specific type of inland water area-rivers designated as free-flowing. Out of a global total of 11.7 million kilometers of rivers, 1.9 million kilometers (16%) are within protected areas and 10.1 million kilometers are classified as free-flowing, with 1.7 million kilometers of the free-flowing kilometers (17%) within protected areas. Thus, at the global level, the proportion of rivers in protected areas is just below the Aichi Target, and the proportion of free-flowing rivers within protected areas equals that target. However, the extent of protection varies widely across river basins, countries, and continents, and many of these geographic units have a level of protection far lower than the target. Further, high discharge mainstem rivers tend to have lower extent of protection. We conclude by reviewing the limitations of measuring river protection by the proportion of river kilometers within protected areas and describe a range of mechanisms that can provide more effective protection. We also propose a set of recommendations for a more comprehensive quantification of global river protection.
Life for many of the world's marine fish begins at the ocean surface. Ocean conditions dictate food availability and govern survivorship, yet little is known about the habitat preferences of larval fish during this highly vulnerable life-history stage. Here we show that surface slicks, a ubiquitous coastal ocean convergence feature, are important nurseries for larval fish from many ocean habitats at ecosystem scales. Slicks had higher densities of marine phytoplankton (1.7-fold), zooplankton (larval fish prey; 3.7-fold), and larval fish (8.1-fold) than nearby ambient waters across our study region in Hawai'i. Slicks contained larger, more well-developed individuals with competent swimming abilities compared to ambient waters, suggesting a physiological benefit to increased prey resources. Slicks also disproportionately accumulated prey-size plastics, resulting in a 60-fold higher ratio of plastics to larval fish prey than nearby waters. Dissections of hundreds of larval fish found that 8.6% of individuals in slicks had ingested plastics, a 2.3-fold higher occurrence than larval fish from ambient waters. Plastics were found in 7 of 8 families dissected, including swordfish (Xiphiidae), a commercially targeted species, and flying fish (Exocoetidae), a principal prey item for tuna and seabirds. Scaling up across an ∼1,000 km2 coastal ecosystem in Hawai'i revealed slicks occupied only 8.3% of ocean surface habitat but contained 42.3% of all neustonic larval fish and 91.8% of all floating plastics. The ingestion of plastics by larval fish could reduce survivorship, compounding threats to fisheries productivity posed by overfishing, climate change, and habitat loss.
Resilience underpins the sustainability of both ecological and social systems. Extensive loss of reef corals following recent mass bleaching events have challenged the notion that support of system resilience is a viable reef management strategy. While resilience-based management (RBM) cannot prevent the damaging effects of major disturbances, such as mass bleaching events, it can support natural processes that promote resistance and recovery. Here, we review the potential of RBM to help sustain coral reefs in the 21st century. We explore the scope for supporting resilience through existing management approaches and emerging technologies and discuss their opportunities and limitations in a changing climate. We argue that for RBM to be effective in a changing world, reef management strategies need to involve both existing and new interventions that together reduce stress, support the fitness of populations and species, and help people and economies to adapt to a highly altered ecosystem.
Despite the unique nature of endemic species, their origin and population history remain poorly studied. We investigated the population history of 28 coral reef fish species, close related, from the Gambier and Marquesas Islands, from five families, with range size varying from widespread to small-range endemic. We analyzed both mitochondrial and nuclear sequence data using neutrality test and Bayesian analysis (EBSP and ABC). We found evidence for demographic expansions for most species (24 of 28), irrespective of range size, reproduction strategy or archipelago. The timing of the expansions varied greatly among species, from 8,000 to 2,000,000 years ago. The typical hypothesis for reef fish that links population expansions to the Last Glacial Maximum fit for 14 of the 24 demographic expansions. We propose two evolutionary processes that could lead to expansions older than the LGM: (a) we are retrieving the signature of an old colonization process for widespread, large-range endemic and paleoendemic species or (b) speciation; the expansion reflects the birth of the species for neoendemic species. We show for the first time that the demographic histories of endemic and widespread reef fish are not distinctly different and suggest that a number of processes drive endemism.
Clonal populations are often characterized by reduced levels of genotypic diversity, which can translate into lower numbers of functional phenotypes, both of which impede adaptation. Study of partially clonal animals enables examination of the environmental settings under which clonal reproduction is favoured. Here, we gathered genotypic and phenotypic information from 3,651 georeferenced colonies of the fire coral Millepora platyphylla in five habitats with different hydrodynamic regimes in Moorea, French Polynesia. In the upper slope where waves break, most colonies grew as vertical sheets ("sheet tree") making them more vulnerable to fragmentation. Nearly all fire corals in the other habitats are encrusting or massive. The M. platyphylla population is highly clonal (80% of the colonies are clones), while characterized by the highest genotype diversity ever documented for terrestrial or marine populations (1,064 genotypes). The proportion of clones varies greatly among habitats (≥58%-97%) and clones (328 clonal lineages) are distributed perpendicularly from the reef crest, perfectly aligned with wave energy. There are six clonal lineages with clones dispersed in at least two adjacent habitats that strongly demonstrate phenotypic plasticity. Eighty per cent of the colonies in these lineages are "sheet tree" on the upper slope, while 80%-100% are encrusting or massive on the mid slope and back reef. This is a unique example of phenotypic plasticity among reef-building coral clones as corals typically have wave-tolerant growth forms in high-energy reef areas.
Losses of corals worldwide emphasize the need to understand what drives reef decline. Stressors such as overfishing and nutrient pollution may reduce resilience of coral reefs by increasing coral–algal competition and reducing coral recruitment, growth and survivorship. Such effects may themselves develop via several mechanisms, including disruption of coral microbiomes. Here we report the results of a 3-year field experiment simulating overfishing and nutrient pollution. These stressors increase turf and macroalgal cover, destabilizing microbiomes, elevating putative pathogen loads, increasing disease more than twofold and increasing mortality up to eightfold. Above-average temperatures exacerbate these effects, further disrupting microbiomes of unhealthy corals and concentrating 80% of mortality in the warmest seasons. Surprisingly, nutrients also increase bacterial opportunism and mortality in corals bitten by parrotfish, turning normal trophic interactions deadly for corals. Thus, overfishing and nutrient pollution impact reefs down to microbial scales, killing corals by sensitizing them to predation, above-average temperatures and bacterial opportunism.
19, 54, 55); Roger Beeden (page 21); Anna Dowd (page 26
Infectious marine diseases can decimate populations and are increasing among some taxa due to global change and our increasing reliance on marine environments. Marine diseases become emergencies when significant ecological, economic or social impacts occur. We can prepare for and manage these emergencies through improved surveillance, and the development and iterative refinement of approaches to mitigate disease and its impacts. Improving surveillance requires fast, accurate diagnoses, forecasting disease risk and real-time monitoring of disease-promoting environmental conditions. Diversifying impact mitigation involves increasing host resilience to disease, reducing pathogen abundance and managing environmental factors that facilitate disease. Disease surveillance and mitigation can be adaptive if informed by research advances and catalysed by communication among observers, researchers and decision-makers using information-sharing platforms. Recent increases in the awareness of the threats posed by marine diseases may lead to policy frameworks that facilitate the responses and management that marine disease emergencies require.
Natal philopatry, the return of individuals to their natal area for reproduction, has advantages and disadvantages for animal populations. Natal philopatry may generate local genetic adaptation, but it may also increase the probability of inbreeding that can compromise persistence. Although natal philopatry is well documented in anadromous fishes, marine fish may also return to their birth site to spawn. How philopatry shapes wild fish populations is, however, unclear because it requires constructing multigenerational pedigrees that are currently lacking for marine fishes. Here we present the first multigenerational pedigree for a marine fish population by repeatedly genotyping all individuals in a population of the orange clownfish (Amphiprion percula) at Kimbe Island (Papua New Guinea) during a 10-y period. Based on 2927 individuals, our pedigree analysis revealed that longitudinal philopatry was recurrent over five generations. Progeny tended to settle close to their parents, with related individuals often sharing the same colony. However, successful inbreeding was rare, and genetic diversity remained high, suggesting occasional inbreeding does not impair local population persistence. Local reproductive success was dependent on the habitat larvae settled into, rather than the habitat they came from. Our study suggests that longitudinal philopatry can influence both population replenishment and local adaptation of marine fishes. Resolving multigenerational pedigrees during a relatively short period, as we present here, provides a framework for assessing the ability of marine populations to persist and adapt to accelerating climate change.
The extent of the global human footprint [1] limits our understanding of what is natural in the marine environment. Remote, near-pristine areas provide some baseline expectations for biomass [2, 3] and suggest that predators dominate, producing an inverted biomass pyramid. The southern pass of Fakarava atoll a biosphere reserve in French Polynesia hosts an average of 600 reef sharks, two to three times the biomass per hectare documented for any other reef shark aggregations [4]. This huge biomass of predators makes the trophic pyramid inverted. Bioenergetics models indicate that the sharks require similar to 90 tons of fish per year, whereas the total fish production in the pass is similar to 17 tons per year. Energetic theory shows that such trophic structure is maintained through subsidies [5-9], and empirical evidence suggests that sharks must engage in wide-ranging foraging excursions to meet energy needs [9, 10]. We used underwater surveys and acoustic telemetry to assess shark residency in the pass and feeding behavior and used bioenergetics models to understand energy flow. Contrary to previous findings, our results highlight that sharks may overcome low local energy availability by feeding on fish spawning aggregations, which concentrate energy from other local trophic pyramids. Fish spawning aggregations are known to be targeted by sharks, but they were previously believed to play a minor role representing occasional opportunistic supplements. This research demonstrates that fish spawning aggregations can play a significant role in the maintenance of local inverted pyramids in pristine marine areas. Conservation of fish spawning aggregations can help conserve shark populations, especially if combined with shark fishing bans.
Coral reefs across the world’s oceans are in the midst of the longest bleaching event on record (from 2014 to at least 2016). As many of the world’s reefs are remote, there is limited information on how past thermal conditions have influenced reef composition and current stress responses. Using satellite temperature data for 1985–2012, the analysis we present is the first to quantify, for global reef locations, spatial variations in warming trends, thermal stress events and temperature variability at reef-scale (~4 km). Among over 60,000 reef pixels globally, 97% show positive SST trends during the study period with 60% warming significantly. Annual trends exceeded summertime trends at most locations. This indicates that the period of summer-like temperatures has become longer through the record, with a corresponding shortening of the ‘winter’ reprieve from warm temperatures. The frequency of bleaching-level thermal stress increased three-fold between 1985–91 and 2006–12 – a trend climate model projections suggest will continue. The thermal history data products developed enable needed studies relating thermal history to bleaching resistance and community composition. Such analyses can help identify reefs more resilient to thermal stress.
As climate change continues to impact socio-ecological systems, tools that assist conservation managers to understand vulnerability and target adaptations are essential. Quantitative assessments of vulnerability are rare because available frameworks are complex and lack guidance for dealing with data limitations and integrating across scales and disciplines. This paper describes a semi-quantitative method for assessing vulnerability to climate change that integrates socio-ecological factors to address management objectives and support decision-making. The method applies a framework first adopted by the Intergovernmental Panel on Climate Change and uses a structured 10-step process. The scores for each framework element are normalized and multiplied to produce a vulnerability score and then the assessed components are ranked from high to low vulnerability. Sensitivity analyses determine which indicators most influence the analysis and the resultant decision-making process so data quality for these indicators can be reviewed to increase robustness. Prioritisation of components for conservation considers other economic, social and cultural values with vulnerability rankings to target actions that reduce vulnerability to climate change by decreasing exposure or sensitivity and/or increasing adaptive capacity. This framework provides practical decision-support and has been applied to marine ecosystems and fisheries, with two case applications provided as examples: (1) food security in Pacific Island nations under climate-driven fish declines, and (2) fisheries in the Gulf of Carpentaria, northern Australia. The step-wise process outlined here is broadly applicable and can be undertaken with minimal resources using existing data, thereby having great potential to inform adaptive natural resource management in diverse locations.