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.

Complex drivers of invasive macroalgae boom and bust in Kane'ohe Bay, Hawai'i.

Invasive macroalgae Eucheuma sp. and Kappaphycus spp. (E/K) became a dominant benthic feature in Kane'ohe Bay throughout the past four decades - occurring on up to 74 ha of reef area and growing up to three meters thick, which prompted intensive management action. In 2013, E/K cover began decreasing at managed and unmanaged sites. This study examined the extent and timing of the E/K decline and evaluated environmental and ecological drivers beyond management contributing to the decline. E/K continued to recede into 2017 and remains sparse in Kane'ohe Bay today. Increasing over the sampling period, herbivore biomass was negatively correlated with E/K cover, and other significant, non-linear relationships emerged between E/K cover and coral cover, sea surface temperature, wind, and rainfall. This study uncovers several possible mechanisms explaining a boom and bust in E/K abundance, emphasizes the importance of herbivory, and highlights the resilience of coral reefs in Kane'ohe Bay.

Coral reefs benefit from reduced land-sea impacts under ocean warming.

Coral reef ecosystems are being fundamentally restructured by local human impacts and climate-driven marine heatwaves that trigger mass coral bleaching and mortality1. Reducing local impacts can increase reef resistance to and recovery from bleaching2. However, resource managers lack clear advice on targeted actions that best support coral reefs under climate change3 and sector-based governance means most land- and sea-based management efforts remain siloed4. 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 underway5. 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.

Coral taxonomy and local stressors drive bleaching prevalence across the Hawaiian Archipelago in 2019.

The Hawaiian Archipelago experienced a moderate bleaching event in 2019-the third major bleaching event over a 6-year period to impact the islands. In response, the Hawai'i Coral Bleaching Collaborative (HCBC) conducted 2,177 coral bleaching surveys across the Hawaiian Archipelago. The HCBC was established to coordinate bleaching monitoring efforts across the state between academic institutions, non-governmental organizations, and governmental agencies to facilitate data sharing and provide management recommendations. In 2019, the goals of this unique partnership were to: 1) assess the spatial and temporal patterns of thermal stress; 2) examine taxa-level patterns in bleaching susceptibility; 3) quantify spatial variation in bleaching extent; 4) compare 2019 patterns to those of prior bleaching events; 5) identify predictors of bleaching in 2019; and 6) explore site-specific management strategies to mitigate future bleaching events. Both acute thermal stress and bleaching in 2019 were less severe overall compared to the last major marine heatwave events in 2014 and 2015. Bleaching observed was highly site- and taxon-specific, driven by the susceptibility of remaining coral assemblages whose structure was likely shaped by previous bleaching and subsequent mortality. A suite of environmental and anthropogenic predictors was significantly correlated with observed bleaching in 2019. Acute environmental stressors, such as temperature and surface light, were equally important as previous conditions (e.g. historical thermal stress and historical bleaching) in accounting for variation in bleaching during the 2019 event. We found little evidence for acclimation by reefs to thermal stress in the main Hawaiian Islands. Moreover, our findings illustrate how detrimental effects of local anthropogenic stressors, such as tourism and urban run-off, may be exacerbated under high thermal stress. In light of the forecasted increase in severity and frequency of bleaching events, future mitigation of both local and global stressors is a high priority for the future of corals in Hawai'i.

Integrating herbivore assemblages and woody plant cover in an African savanna to reveal how herbivores respond to ecosystem management.

African savannas are experiencing anthropogenically-induced stressors that are accelerating the increase of woody vegetation cover. To combat this, land managers frequently implement large-scale clearing of trees, which can have a cascading influence on mammalian herbivores. Studies rarely focus on how differences in woody cover influence the herbivore assemblage, making it difficult to assess how aggressive measures, or the lack of management, to counteract increasing woody cover affect the local composition and biodiversity of herbivores. We address this knowledge gap by applying a model-based clustering approach to field observations from MalaMala Game Reserve, South Africa to identify multiple herbivore-vegetation 'configurations,' defined as unique sets of herbivore assemblages (i.e., groups of herbivores) associated with differing woody plant covers. Our approach delineated how tree-clearing influences the distribution and abundance of the herbivore community in relation to surrounding savanna areas, which represent a natural mosaic of varying woody cover. Regardless of season, both intensively managed areas cleared of trees and unmanaged areas with high tree cover contained configurations that had depauperate assemblages of herbivores (low species richness, low abundance). By contrast, habitats with intermediate cover of woody vegetation had much higher richness and abundance. These results have substantial implications for managing African savannas in a rapidly changing climate.

Coral-bleaching responses to climate change across biological scales.

The global impacts of climate change are evident in every marine ecosystem. On coral reefs, mass coral bleaching and mortality have emerged as ubiquitous responses to ocean warming, yet one of the greatest challenges of this epiphenomenon is linking information across scientific disciplines and spatial and temporal scales. Here we review some of the seminal and recent coral-bleaching discoveries from an ecological, physiological, and molecular perspective. We also evaluate which data and processes can improve predictive models and provide a conceptual framework that integrates measurements across biological scales. Taking an integrative approach across biological and spatial scales, using for example hierarchical models to estimate major coral-reef processes, will not only rapidly advance coral-reef science but will also provide necessary information to guide decision-making and conservation efforts. To conserve reefs, we encourage implementing mesoscale sanctuaries (thousands of km2 ) that transcend national boundaries. Such networks of protected reefs will provide reef connectivity, through larval dispersal that transverse thermal environments, and genotypic repositories that may become essential units of selection for environmentally diverse locations. Together, multinational networks may be the best chance corals have to persist through climate change, while humanity struggles to reduce emissions of greenhouse gases to net zero.

The transformation of Caribbean coral communities since humans.

The mass die-off of Caribbean corals has transformed many of this region's reefs to macroalgal-dominated habitats since systematic monitoring began in the 1970s. Although attributed to a combination of local and global human stressors, the lack of long-term data on Caribbean reef coral communities has prevented a clear understanding of the causes and consequences of coral declines. We integrated paleoecological, historical, and modern survey data to track the occurrence of major coral species and life-history groups throughout the Caribbean from the prehuman period to the present. The regional loss of Acropora corals beginning by the 1960s from local human disturbances resulted in increases in the occurrence of formerly subdominant stress-tolerant and weedy scleractinian corals and the competitive hydrozoan Millepora beginning in the 1970s and 1980s. These transformations have resulted in the homogenization of coral communities within individual countries. However, increases in stress-tolerant and weedy corals have slowed or reversed since the 1980s and 1990s in tandem with intensified coral bleaching and disease. These patterns reveal the long history of increasingly stressful environmental conditions on Caribbean reefs that began with widespread local human disturbances and have recently culminated in the combined effects of local and global change.

Local conditions magnify coral loss after marine heatwaves.

Climate change threatens coral reefs by causing heat stress events that lead to widespread coral bleaching and mortality. Given the global nature of these mass coral mortality events, recent studies argue that mitigating climate change is the only path to conserve coral reefs. Using a global analysis of 223 sites, we show that local stressors act synergistically with climate change to kill corals. Local factors such as high abundance of macroalgae or urchins magnified coral loss in the year after bleaching. Notably, the combined effects of increasing heat stress and macroalgae intensified coral loss. Our results offer an optimistic premise that effective local management, alongside global efforts to mitigate climate change, can help coral reefs survive the Anthropocene.

Quantifying and addressing the prevalence and bias of study designs in the environmental and social sciences.

Building trust in science and evidence-based decision-making depends heavily on the credibility of studies and their findings. Researchers employ many different study designs that vary in their risk of bias to evaluate the true effect of interventions or impacts. Here, we empirically quantify, on a large scale, the prevalence of different study designs and the magnitude of bias in their estimates. Randomised designs and controlled observational designs with pre-intervention sampling were used by just 23% of intervention studies in biodiversity conservation, and 36% of intervention studies in social science. We demonstrate, through pairwise within-study comparisons across 49 environmental datasets, that these types of designs usually give less biased estimates than simpler observational designs. We propose a model-based approach to combine study estimates that may suffer from different levels of study design bias, discuss the implications for evidence synthesis, and how to facilitate the use of more credible study designs.

Caribbean reefs of the Anthropocene: Variance in ecosystem metrics indicates bright spots on coral depauperate reefs.

Dramatic coral loss has significantly altered many Caribbean reefs, with potentially important consequences for the ecological functions and ecosystem services provided by reef systems. Many studies examine coral loss and its causes-and often presume a universal decline of ecosystem services with coral loss-rather than evaluating the range of possible outcomes for a diversity of ecosystem functions and services at reefs varying in coral cover. We evaluate 10 key ecosystem metrics, relating to a variety of different reef ecosystem functions and services, on 328 Caribbean reefs varying in coral cover. We focus on the range and variability of these metrics rather than on mean responses. In contrast to a prevailing paradigm, we document high variability for a variety of metrics, and for many the range of outcomes is not related to coral cover. We find numerous "bright spots," where herbivorous fish biomass, density of large fishes, fishery value, and/or fish species richness are high, despite low coral cover. Although it remains critical to protect and restore corals, understanding variability in ecosystem metrics among low-coral reefs can facilitate the maintenance of reefs with sustained functions and services as we work to restore degraded systems. This framework can be applied to other ecosystems in the Anthropocene to better understand variance in ecosystem service outcomes and identify where and why bright spots exist.

Widespread loss of Caribbean acroporid corals was underway before coral bleaching and disease outbreaks.

The mass mortality of acroporid corals has transformed Caribbean reefs from coral- to macroalgal-dominated habitats since systematic monitoring began in the 1970s. Declines have been attributed to overfishing, pollution, sea urchin and coral disease, and climate change, but the mechanisms are unresolved due to the dearth of pre-1970s data. We used paleoecological, historical, and survey data to track Acropora presence and dominance throughout the Caribbean from the prehuman period to present. Declines in dominance from prehuman values first occurred in the 1950s for Acropora palmata and the 1960s for Acropora cervicornis, decades before outbreaks of acroporid disease or bleaching. We compared trends in Acropora dominance since 1950 to potential regional and local drivers. Human population negatively affected and consumption of fertilizer for agriculture positively affected A. palmata dominance, the latter likely due to lower human presence in agricultural areas. The earlier, local roots of Caribbean Acropora declines highlight the urgency of mitigating local human impacts.

Nitrogen pollution interacts with heat stress to increase coral bleaching across the seascape.

Climate change is increasing the frequency and magnitude of temperature anomalies that cause coral bleaching, leading to widespread mortality of stony corals that can fundamentally alter reef structure and function. However, bleaching often is spatially variable for a given heat stress event, and drivers of this heterogeneity are not well resolved. While small-scale experiments have shown that excess nitrogen can increase the susceptibility of a coral colony to bleaching, we lack evidence that heterogeneity in nitrogen pollution can shape spatial patterns of coral bleaching across a seascape. Using island-wide surveys of coral bleaching and nitrogen availability within a Bayesian hierarchical modeling framework, we tested the hypothesis that excess nitrogen interacts with temperature anomalies to alter coral bleaching for the two dominant genera of branching corals in Moorea, French Polynesia. For both coral genera, Pocillopora and Acropora, heat stress primarily drove bleaching prevalence (i.e., the proportion of colonies on a reef that bleached). In contrast, the severity of bleaching (i.e., the proportion of an individual colony that bleached) was positively associated with both heat stress and nitrogen availability for both genera. Importantly, nitrogen interacted with heat stress to increase bleaching severity up to twofold when nitrogen was high and heat stress was relatively low. Our finding that excess nitrogen can trigger severe bleaching even under relatively low heat stress implies that mitigating nutrient pollution may enhance the resilience of coral communities in the face of mounting stresses from global climate change.

Parsing human and biophysical drivers of coral reef regimes.

Coral reefs worldwide face unprecedented cumulative anthropogenic effects of interacting local human pressures, global climate change and distal social processes. Reefs are also bound by the natural biophysical environment within which they exist. In this context, a key challenge for effective management is understanding how anthropogenic and biophysical conditions interact to drive distinct coral reef configurations. Here, we use machine learning to conduct explanatory predictions on reef ecosystems defined by both fish and benthic communities. Drawing on the most spatially extensive dataset available across the Hawaiian archipelago-20 anthropogenic and biophysical predictors over 620 survey sites-we model the occurrence of four distinct reef regimes and provide a novel approach to quantify the relative influence of human and environmental variables in shaping reef ecosystems. Our findings highlight the nuances of what underpins different coral reef regimes, the overwhelming importance of biophysical predictors and how a reef's natural setting may either expand or narrow the opportunity space for management interventions. The methods developed through this study can help inform reef practitioners and hold promises for replication across a broad range of ecosystems.

Combining fish and benthic communities into multiple regimes reveals complex reef dynamics.

Coral reefs worldwide face an uncertain future with many reefs reported to transition from being dominated by corals to macroalgae. However, given the complexity and diversity of the ecosystem, research on how regimes vary spatially and temporally is needed. Reef regimes are most often characterised by their benthic components; however, complex dynamics are associated with losses and gains in both fish and benthic assemblages. To capture this complexity, we synthesised 3,345 surveys from Hawai'i to define reef regimes in terms of both fish and benthic assemblages. Model-based clustering revealed five distinct regimes that varied ecologically, and were spatially heterogeneous by island, depth and exposure. We identified a regime characteristic of a degraded state with low coral cover and fish biomass, one that had low coral but high fish biomass, as well as three other regimes that varied significantly in their ecology but were previously considered a single coral dominated regime. Analyses of time series data reflected complex system dynamics, with multiple transitions among regimes that were a function of both local and global stressors. Coupling fish and benthic communities into reef regimes to capture complex dynamics holds promise for monitoring reef change and guiding ecosystem-based management of coral reefs.

Advancing the integration of spatial data to map human and natural drivers on coral reefs.

A major challenge for coral reef conservation and management is understanding how a wide range of interacting human and natural drivers cumulatively impact and shape these ecosystems. Despite the importance of understanding these interactions, a methodological framework to synthesize spatially explicit data of such drivers is lacking. To fill this gap, we established a transferable data synthesis methodology to integrate spatial data on environmental and anthropogenic drivers of coral reefs, and applied this methodology to a case study location-the Main Hawaiian Islands (MHI). Environmental drivers were derived from time series (2002-2013) of climatological ranges and anomalies of remotely sensed sea surface temperature, chlorophyll-a, irradiance, and wave power. Anthropogenic drivers were characterized using empirically derived and modeled datasets of spatial fisheries catch, sedimentation, nutrient input, new development, habitat modification, and invasive species. Within our case study system, resulting driver maps showed high spatial heterogeneity across the MHI, with anthropogenic drivers generally greatest and most widespread on O'ahu, where 70% of the state's population resides, while sedimentation and nutrients were dominant in less populated islands. Together, the spatial integration of environmental and anthropogenic driver data described here provides a first-ever synthetic approach to visualize how the drivers of coral reef state vary in space and demonstrates a methodological framework for implementation of this approach in other regions of the world. By quantifying and synthesizing spatial drivers of change on coral reefs, we provide an avenue for further research to understand how drivers determine reef diversity and resilience, which can ultimately inform policies to protect coral reefs.

Correction: Largest global shark biomass found in the northern Galápagos Islands of Darwin and Wolf.

[This corrects the article DOI: 10.7717/peerj.1911.].

Seascape models reveal places to focus coastal fisheries management.

To design effective marine reserves and support fisheries, more information on fishing patterns and impacts for targeted species is needed, as well as better understanding of their key habitats. However, fishing impacts vary geographically and are difficult to disentangle from other factors that influence targeted fish distributions. We developed a set of fishing effort and habitat layers at high resolution and employed machine learning techniques to create regional-scale seascape models and predictive maps of biomass and body length of targeted reef fishes for the main Hawaiian Islands. Spatial patterns of fishing effort were shown to be highly variable and seascape models indicated a low threshold beyond which targeted fish assemblages were severely impacted. Topographic complexity, exposure, depth, and wave power were identified as key habitat variables that influenced targeted fish distributions and defined productive habitats for reef fisheries. High targeted reef fish biomass and body length were found in areas not easily accessed by humans, while model predictions when fishing effort was set to zero showed these high values to be more widely dispersed among suitable habitats. By comparing current targeted fish distributions with those predicted when fishing effort was removed, areas with high recovery potential on each island were revealed, with average biomass recovery of 517% and mean body length increases of 59% on Oahu, the most heavily fished island. Spatial protection of these areas would aid recovery of nearshore coral reef fisheries.

Managing Local Stressors for Coral Reef Condition and Ecosystem Services Delivery Under Climate Scenarios.

Coral reefs provide numerous ecosystem goods and services, but are threatened by multiple environmental and anthropogenic stressors. To identify management scenarios that will reverse or mitigate ecosystem degradation, managers can benefit from tools that can quantify projected changes in ecosystem services due to alternative management options. We used a spatially-explicit biophysical ecosystem model to evaluate socio-ecological trade-offs of land-based vs. marine-based management scenarios, and local-scale vs. global-scale stressors and their cumulative impacts. To increase the relevance of understanding ecological change for the public and decision-makers, we used four ecological production functions to translate the model outputs into the ecosystem services: "State of the Reef," "Trophic Integrity," "Fisheries Production," and "Fisheries Landings." For a case study of Maui Nui, Hawai'i, land-based management attenuated coral cover decline whereas fisheries management promoted higher total fish biomass. Placement of no-take marine protected areas (MPAs) across 30% of coral reef areas led to a reversal of the historical decline in predatory fish biomass, although this outcome depended on the spatial arrangement of MPAs. Coral cover declined less severely under strict sediment mitigation scenarios. However, the benefits of these local management scenarios were largely lost when accounting for climate-related impacts. Climate-related stressors indirectly increased herbivore biomass due to the shift from corals to algae and, hence, greater food availability. The two ecosystem services related to fish biomass increased under climate-related stressors but "Trophic Integrity" of the reef declined, indicating a less resilient reef. "State of the Reef" improved most and "Trophic Integrity" declined least under an optimistic global warming scenario and strict local management. This work provides insight into the relative influence of land-based vs. marine-based management and local vs. global stressors as drivers of changes in ecosystem dynamics while quantifying the tradeoffs between conservation- and extraction-oriented ecosystem services.

Largest global shark biomass found in the northern Galápagos Islands of Darwin and Wolf.

Overfishing has dramatically depleted sharks and other large predatory fishes worldwide except for a few remote and/or well-protected areas. The islands of Darwin and Wolf in the far north of the Galapagos Marine Reserve (GMR) are known for their large shark abundance, making them a global scuba diving and conservation hotspot. Here we report quantitative estimates of fish abundance at Darwin and Wolf over two consecutive years using stereo-video surveys, which reveal the largest reef fish biomass ever reported (17.5 t [Formula: see text] on average), consisting largely of sharks. Despite this, the abundance of reef fishes around the GMR, such as groupers, has been severely reduced because of unsustainable fishing practices. Although Darwin and Wolf are within the GMR, they were not fully protected from fishing until March 2016. Given the ecological value and the economic importance of Darwin and Wolf for the dive tourism industry, the current protection should ensure the long-term conservation of this hotspot of unique global value.

Effects of Gear Restriction on the Abundance of Juvenile Fishes along Sandy Beaches in Hawai'i.

In 2007, due to growing concerns of declines in nearshore fisheries in Hawai'i, a ban on gillnets was implemented in designated areas around the island of O'ahu in the main Hawaiian Islands. Utilizing a 17 year time-series of juvenile fish abundance beginning prior to the implementation of the gillnet ban, we examined the effects of the ban on the abundance of juveniles of soft-bottom associated fish species. Using a Before-After-Control-Impact (BACI) sampling design, we compared the abundance of targeted fishery species in a bay where gillnet fishing was banned (Kailua, O'ahu), and an adjacent bay where fishing is still permitted (Waimanalo, O'ahu). Our results show that when multiple juvenile fish species were combined, abundance declined over time in both locations, but the pattern varied for each of the four species groups examined. Bonefishes were the only species group with a significant BACI effect, with higher abundance in Kailua in the period after the gillnet ban. This study addressed a need for scientific assessment of a fisheries regulation that is rarely possible due to lack of quality data before enactment of such restrictions. Thus, we developed a baseline status of juveniles of an important fishery species, and found effects of a fishery management regulation in Hawai'i.