Environmental drivers of coral reef carbonate production and bioerosion: a multi-scale analysis.

The resilience of coral reefs depends on the balance between reef growth and reef breakdown, and their responses to changing environmental conditions. Across the 2500-km Hawaiian Archipelago, we quantified rates of carbonate production, bioerosion, and net accretion at regional, island, site, and within-site spatial scales and tested how these rates respond to environmental conditions across different spatial scales. Overall, there were four major outcomes from this study: (1) bioerosion rates were generally higher in the populated Main Hawaiian Islands (MHI) than the remote, protected Northwestern Hawaiian Islands (NWHI), while carbonate production rates did not vary significantly between the two regions; (2) variability in carbonate production, bioerosion, and net accretion rates was greatest at the smallest within-reef spatial scale; (3) carbonate production and bioerosion rates were associated with distinct sets of environmental parameters; and (4) the strongest correlates of carbonate production, bioerosion, and net accretion rates were different between the MHI region and the NWHI region: in the MHI, the dominant correlates were percent cover of macroalgae and herbivorous fish biomass for carbonate production and bioerosion, respectively, whereas in the NWHI, the top correlates were total alkalinity and benthic cover. This study highlights the need to understand accretion and erosion processes as well as local environmental conditions to predict net coral reef responses to future environmental changes.

Fishing degrades size structure of coral reef fish communities.

Fishing pressure on coral reef ecosystems has been frequently linked to reductions of large fishes and reef fish biomass. Associated impacts on overall community structure are, however, less clear. In size-structured aquatic ecosystems, fishing impacts are commonly quantified using size spectra, which describe the distribution of individual body sizes within a community. We examined the size spectra and biomass of coral reef fish communities at 38 US-affiliated Pacific islands that ranged in human presence from near pristine to human population centers. Size spectra 'steepened' steadily with increasing human population and proximity to market due to a reduction in the relative biomass of large fishes and an increase in the dominance of small fishes. Reef fish biomass was substantially lower on inhabited islands than uninhabited ones, even at inhabited islands with the lowest levels of human presence. We found that on populated islands size spectra exponents decreased (analogous to size spectra steepening) linearly with declining biomass, whereas on uninhabited islands there was no relationship. Size spectra were steeper in regions of low sea surface temperature but were insensitive to variation in other environmental and geomorphic covariates. In contrast, reef fish biomass was highly sensitive to oceanographic conditions, being influenced by both oceanic productivity and sea surface temperature. Our results suggest that community size structure may be a more robust indicator than fish biomass to increasing human presence and that size spectra are reliable indicators of exploitation impacts across regions of different fish community compositions, environmental drivers, and fisheries types. Size-based approaches that link directly to functional properties of fish communities, and are relatively insensitive to abiotic variation across biogeographic regions, offer great potential for developing our understanding of fishing impacts in coral reef ecosystems.

Commonness and rarity in the marine biosphere.

Explaining patterns of commonness and rarity is fundamental for understanding and managing biodiversity. Consequently, a key test of biodiversity theory has been how well ecological models reproduce empirical distributions of species abundances. However, ecological models with very different assumptions can predict similar species abundance distributions, whereas models with similar assumptions may generate very different predictions. This complicates inferring processes driving community structure from model fits to data. Here, we use an approximation that captures common features of "neutral" biodiversity models--which assume ecological equivalence of species--to test whether neutrality is consistent with patterns of commonness and rarity in the marine biosphere. We do this by analyzing 1,185 species abundance distributions from 14 marine ecosystems ranging from intertidal habitats to abyssal depths, and from the tropics to polar regions. Neutrality performs substantially worse than a classical nonneutral alternative: empirical data consistently show greater heterogeneity of species abundances than expected under neutrality. Poor performance of neutral theory is driven by its consistent inability to capture the dominance of the communities' most-abundant species. Previous tests showing poor performance of a neutral model for a particular system often have been followed by controversy about whether an alternative formulation of neutral theory could explain the data after all. However, our approach focuses on common features of neutral models, revealing discrepancies with a broad range of empirical abundance distributions. These findings highlight the need for biodiversity theory in which ecological differences among species, such as niche differences and demographic trade-offs, play a central role.

Energetic differences between bacterioplankton trophic groups and coral reef resistance.

Coral reefs are among the most productive and diverse marine ecosystems on the Earth. They are also particularly sensitive to changing energetic requirements by different trophic levels. Microbialization specifically refers to the increase in the energetic metabolic demands of microbes relative to macrobes and is significantly correlated with increasing human influence on coral reefs. In this study, metabolic theory of ecology is used to quantify the relative contributions of two broad bacterioplankton groups, autotrophs and heterotrophs, to energy flux on 27 Pacific coral reef ecosystems experiencing human impact to varying degrees. The effective activation energy required for photosynthesis is lower than the average energy of activation for the biochemical reactions of the Krebs cycle, and changes in the proportional abundance of these two groups can greatly affect rates of energy and materials cycling. We show that reef-water communities with a higher proportional abundance of microbial autotrophs expend more metabolic energy per gram of microbial biomass. Increased energy and materials flux through fast energy channels (i.e. water-column associated microbial autotrophs) may dampen the detrimental effects of increased heterotrophic loads (e.g. coral disease) on coral reef systems experiencing anthropogenic disturbance.

Incorporating climate and ocean change into extinction risk assessments for 82 coral species.

Many marine invertebrate species facing potential extinction have uncertain taxonomies and poorly known demographic and ecological traits. Uncertainties are compounded when potential extinction drivers are climate and ocean changes whose effects on even widespread and abundant species are only partially understood. The U.S. Endangered Species Act mandates conservation management decisions founded on the extinction risk to species based on the best available science at the time of consideration-requiring prompt action rather than awaiting better information. We developed an expert-opinion threat-based approach that entails a structured voting system to assess extinction risk from climate and ocean changes and other threats to 82 coral species for which population status and threat response information was limited. Such methods are urgently needed because constrained budgets and manpower will continue to hinder the availability of desired data for many potentially vulnerable marine species. Significant species-specific information gaps and uncertainties precluded quantitative assessments of habitat loss or population declines and necessitated increased reliance on demographic characteristics and threat vulnerabilities at genus or family levels. Adapting some methods (e.g., a structured voting system) used during other assessments and developing some new approaches (e.g., integrated assessment of threats and demographic characteristics), we rated the importance of threats contributing to coral extinction risk and assessed those threats against population status and trend information to evaluate each species' extinction risk over the 21st century. This qualitative assessment resulted in a ranking with an uncertainty range for each species according to their estimated likelihood of extinction. We offer guidance on approaches for future biological extinction risk assessments, especially in cases of data-limited species likely to be affected by global-scale threats. Incorporación del Cambio Climático y Oceánico en Estudios de Riesgo de Extinción para 82 Especies de Coral.

Re-creating missing population baselines for Pacific reef sharks.

Sharks and other large predators are scarce on most coral reefs, but studies of their historical ecology provide qualitative evidence that predators were once numerous in these ecosystems. Quantifying density of sharks in the absence of humans (baseline) is, however, hindered by a paucity of pertinent time-series data. Recently researchers have used underwater visual surveys, primarily of limited spatial extent or nonstandard design, to infer negative associations between reef shark abundance and human populations. We analyzed data from 1607 towed-diver surveys (>1 ha transects surveyed by observers towed behind a boat) conducted at 46 reefs in the central-western Pacific Ocean, reefs that included some of the world's most pristine coral reefs. Estimates of shark density from towed-diver surveys were substantially lower (<10%) than published estimates from surveys along small transects (<0.02 ha), which is not consistent with inverted biomass pyramids (predator biomass greater than prey biomass) reported by other researchers for pristine reefs. We examined the relation between the density of reef sharks observed in towed-diver surveys and human population in models that accounted for the influence of oceanic primary productivity, sea surface temperature, reef area, and reef physical complexity. We used these models to estimate the density of sharks in the absence of humans. Densities of gray reef sharks (Carcharhinus amblyrhynchos), whitetip reef sharks (Triaenodon obesus), and the group "all reef sharks" increased substantially as human population decreased and as primary productivity and minimum sea surface temperature (or reef area, which was highly correlated with temperature) increased. Simulated baseline densities of reef sharks under the absence of humans were 1.1-2.4/ha for the main Hawaiian Islands, 1.2-2.4/ha for inhabited islands of American Samoa, and 0.9-2.1/ha for inhabited islands in the Mariana Archipelago, which suggests that density of reef sharks has declined to 3-10% of baseline levels in these areas.

Densities and drivers of sea turtle populations across Pacific coral reef ecosystems.

Sea turtle populations are often assessed at the regional to sub-basin scale from discrete indices of nesting abundance. While this may be practical and sometimes effective, widespread in-water surveys may enhance assessments by including additional demographics, locations, and revealing emerging population trends. Here, we describe sea turtle observations from 13 years of towed-diver surveys across 53 coral islands, atolls, and reefs in the Central, West, and South Pacific. These surveys covered more than 7,300 linear km, and observed more than 3,400 green (Chelonia mydas) and hawksbill (Eretmochelys imbricata) sea turtles. From these data, we estimated sea turtle densities, described trends across space and time, and modelled the influence of environmental and anthropogenic drivers. Both species were patchily distributed across spatial scales, and green turtles were 11 times more abundant than hawksbills. The Pacific Remote Island Areas had the highest densities of greens (3.62 turtles km-1, Jarvis Island), while American Samoa had the most hawksbills (0.12 turtles km-1, Ta'u Island). The Hawaiian Islands had the lowest turtle densities (island ave = 0.07 turtles km-1) yet the highest annual population growth (µ = 0.08, σ = 0.22), suggesting extensive management protections can yield positive conservation results. Densities peaked at 27.5°C SST, in areas of high productivity and low human impact, and were consistent with patterns of historic overexploitation. Though such intensive surveys have great value, they are logistically demanding and therefore have an uncertain budget and programmatic future. We hope the methods we described here may be applied to future comparatively low-cost surveys either with autonomous vehicles or with environmental DNA.

The Rarity of Depth Refugia from Coral Bleaching Heat Stress in the Western and Central Pacific Islands.

Some researchers have suggested that corals living in deeper reefs may escape heat stress experienced by shallow corals. We evaluated the potential of deep coral reef refugia from bleaching stress by leveraging a long record of satellite-derived sea surface temperature data with a temporal, spatial, and depth precision of in situ temperature records. We calculated an in situ stress metric using a depth bias-adjusted threshold for 457 coral reef sites among 49 islands in the western and central Pacific Ocean over the period 2001-2017. Analysis of 1,453 heating events found no meaningful depth refuge from heat stress down to 38 m, and no significant association between depth and subsurface heat stress. Further, the surface metric underestimated subsurface stress by an average of 39.3%, across all depths. Combining satellite and in situ temperature data can provide bleaching-relevant heat stress results to avoid misrepresentation of heat stress exposure at shallow reefs.

An ecological acoustic recorder (EAR) for long-term monitoring of biological and anthropogenic sounds on coral reefs and other marine habitats.

Keeping track of long-term biological trends in many marine habitats is a challenging task that is exacerbated when the habitats in question are in remote locations. Monitoring the ambient sound field may be a useful way of assessing biological activity because many behavioral processes are accompanied by sound production. This article reports the preliminary results of an effort to develop and use an Ecological Acoustic Recorder (EAR) to monitor biological activity on coral reefs and in surrounding waters for periods of 1 year or longer. The EAR is a microprocessor-based autonomous recorder that periodically samples the ambient sound field and also automatically detects sounds that meet specific criteria. The system was used to record the sound field of coral reefs and other marine habitats on Oahu, HI. Snapping shrimp produced the dominant acoustic energy on the reefs examined and exhibited clear diel acoustic trends. Other biological sounds recorded included those produced by fish and cetaceans, which also exhibited distinct temporal variability. Motor vessel activity could also be monitored effectively with the EAR. The results indicate that acoustic monitoring may be an effective means of tracking biological and anthropogenic activity at locations where continuous monitoring by traditional survey methods is impractical.

Repeat bleaching of a central Pacific coral reef over the past six decades (1960-2016).

The oceans are warming and coral reefs are bleaching with increased frequency and severity, fueling concerns for their survival through this century. Yet in the central equatorial Pacific, some of the world's most productive reefs regularly experience extreme heat associated with El Niño. Here we use skeletal signatures preserved in long-lived corals on Jarvis Island to evaluate the coral community response to multiple successive heatwaves since 1960. By tracking skeletal stress band formation through the 2015-16 El Nino, which killed 95% of Jarvis corals, we validate their utility as proxies of bleaching severity and show that 2015-16 was not the first catastrophic bleaching event on Jarvis. Since 1960, eight severe (>30% bleaching) and two moderate (<30% bleaching) events occurred, each coinciding with El Niño. While the frequency and severity of bleaching on Jarvis did not increase over this time period, 2015-16 was unprecedented in magnitude. The trajectory of recovery of this historically resilient ecosystem will provide critical insights into the potential for coral reef resilience in a warming world.

Marine debris collects within the North Pacific Subtropical Convergence Zone.

Floating marine debris, particularly derelict fishing gear, is a hazard to fish, marine mammals, turtles, sea birds, coral reefs, and even human activities. To ameliorate the economic and environmental impact of marine debris, we need to efficiently locate and retrieve dangerous debris at sea. Guided by satellite-derived information, we made four flights north of Hawaii in March and April 2005. During these aerial surveys, we observed over 1800 individual pieces of debris, including 122 derelict fishing nets. The largest debris concentrations were found just north of the North Pacific Transition Zone Chlorophyll Front (TZCF) within the North Pacific Subtropical Convergence Zone (STCZ). Debris densities were significantly correlated with sea-surface temperature (SST), chlorophyll-a concentration (Chla), and the gradient of Chla. A Debris Estimated Likelihood Index (DELI) was developed to predict where high concentrations of debris would be most likely in the North Pacific during spring and early summer.

Long-term monitoring of coral reef fish assemblages in the Western central pacific.

Throughout the tropics, coral reef ecosystems, which are critically important to people, have been greatly altered by humans. Differentiating human impacts from natural drivers of ecosystem state is essential to effective management. Here we present a dataset from a large-scale monitoring program that surveys coral reef fish assemblages and habitats encompassing the bulk of the US-affiliated tropical Pacific, and spanning wide gradients in both natural drivers and human impact. Currently, this includes >5,500 surveys from 39 islands and atolls in Hawaii (including the main and Northwestern Hawaiian Islands) and affiliated geo-political regions of American Samoa, the Commonwealth of the Northern Mariana Islands, Guam, and the Pacific Remote Islands Areas. The dataset spans 2010-2017, during which time, each region was visited at least every three years, and ~500-1,000 surveys performed annually. This standardised dataset is a powerful resource that can be used to understand how human, environmental and oceanographic conditions influence coral reef fish community structure and function, providing a basis for research to support effective management outcomes.

Management Strategy Evaluation Applied to Coral Reef Ecosystems in Support of Ecosystem-Based Management.

Ecosystem modelling is increasingly used to explore ecosystem-level effects of changing environmental conditions and management actions. For coral reefs there has been increasing interest in recent decades in the use of ecosystem models for evaluating the effects of fishing and the efficacy of marine protected areas. However, ecosystem models that integrate physical forcings, biogeochemical and ecological dynamics, and human induced perturbations are still underdeveloped. We applied an ecosystem model (Atlantis) to the coral reef ecosystem of Guam using a suite of management scenarios prioritized in consultation with local resource managers to review the effects of each scenario on performance measures related to the ecosystem, the reef-fish fishery (e.g., fish landings) and coral habitat. Comparing tradeoffs across the selected scenarios showed that each scenario performed best for at least one of the selected performance indicators. The integrated 'full regulation' scenario outperformed other scenarios with four out of the six performance metrics at the cost of reef-fish landings. This model application quantifies the socio-ecological costs and benefits of alternative management scenarios. When the effects of climate change were taken into account, several scenarios performed equally well, but none prevented a collapse in coral biomass over the next few decades assuming a business-as-usual greenhouse gas emissions scenario.

An Integrated Coral Reef Ecosystem Model to Support Resource Management under a Changing Climate.

Millions of people rely on the ecosystem services provided by coral reefs, but sustaining these benefits requires an understanding of how reefs and their biotic communities are affected by local human-induced disturbances and global climate change. Ecosystem-based management that explicitly considers the indirect and cumulative effects of multiple disturbances has been recommended and adopted in policies in many places around the globe. Ecosystem models give insight into complex reef dynamics and their responses to multiple disturbances and are useful tools to support planning and implementation of ecosystem-based management. We adapted the Atlantis Ecosystem Model to incorporate key dynamics for a coral reef ecosystem around Guam in the tropical western Pacific. We used this model to quantify the effects of predicted climate and ocean changes and current levels of current land-based sources of pollution (LBSP) and fishing. We used the following six ecosystem metrics as indicators of ecosystem state, resilience and harvest potential: 1) ratio of calcifying to non-calcifying benthic groups, 2) trophic level of the community, 3) biomass of apex predators, 4) biomass of herbivorous fishes, 5) total biomass of living groups and 6) the end-to-start ratio of exploited fish groups. Simulation tests of the effects of each of the three drivers separately suggest that by mid-century climate change will have the largest overall effect on this suite of ecosystem metrics due to substantial negative effects on coral cover. The effects of fishing were also important, negatively influencing five out of the six metrics. Moreover, LBSP exacerbates this effect for all metrics but not quite as badly as would be expected under additive assumptions, although the magnitude of the effects of LBSP are sensitive to uncertainty associated with primary productivity. Over longer time spans (i.e., 65 year simulations), climate change impacts have a slight positive interaction with other drivers, generally meaning that declines in ecosystem metrics are not as steep as the sum of individual effects of the drivers. These analyses offer one way to quantify impacts and interactions of particular stressors in an ecosystem context and so provide guidance to managers. For example, the model showed that improving water quality, rather than prohibiting fishing, extended the timescales over which corals can maintain high abundance by at least 5-8 years. This result, in turn, provides more scope for corals to adapt or for resilient species to become established and for local and global management efforts to reduce or reverse stressors.

Baseline Assessment of Net Calcium Carbonate Accretion Rates on U.S. Pacific Reefs.

This paper presents a comprehensive quantitative baseline assessment of in situ net calcium carbonate accretion rates (g CaCO3 cm(-2) yr(-1)) of early successional recruitment communities on Calcification Accretion Unit (CAU) plates deployed on coral reefs at 78 discrete sites, across 11 islands in the central and south Pacific Oceans. Accretion rates varied substantially within and between islands, reef zones, levels of wave exposure, and island geomorphology. For forereef sites, mean accretion rates were the highest at Rose Atoll, Jarvis, and Swains Islands, and the lowest at Johnston Atoll and Tutuila. A comparison between reef zones showed higher accretion rates on forereefs compared to lagoon sites; mean accretion rates were also higher on windward than leeward sites but only for a subset of islands. High levels of spatial variability in net carbonate accretion rates reported herein draw attention to the heterogeneity of the community assemblages. Percent cover of key early successional taxa on CAU plates did not reflect that of the mature communities present on surrounding benthos, possibly due to the short deployment period (2 years) of the experimental units. Yet, net CaCO3 accretion rates were positively correlated with crustose coralline algae (CCA) percent cover on the surrounding benthos and on the CAU plates, which on average represented >70% of the accreted material. For foreeefs and lagoon sites combined CaCO3 accretion rates were statistically correlated with total alkalinity and Chlorophyll-a; a GAM analysis indicated that SiOH and Halimeda were the best predictor variables of accretion rates on lagoon sites, and total alkalinity and Chlorophyll-a for forereef sites, demonstrating the utility of CAUs as a tool to monitor changes in reef accretion rates as they relate to ocean acidification. This study underscores the pivotal role CCA play as a key benthic component and supporting actively calcifying reefs; high Mg-calcite exoskeletons makes CCA extremely susceptible changes in ocean water pH, emphasizing the far-reaching threat that ocean acidification poses to the ecological function and persistence of coral reefs worldwide.

Human, oceanographic and habitat drivers of central and western Pacific coral reef fish assemblages.

Coral reefs around US- and US-affiliated Pacific islands and atolls span wide oceanographic gradients and levels of human impact. Here we examine the relative influence of these factors on coral reef fish biomass, using data from a consistent large-scale ecosystem monitoring program conducted by scientific divers over the course of >2,000 hours of underwater observation at 1,934 sites, across ~40 islands and atolls. Consistent with previous smaller-scale studies, our results show sharp declines in reef fish biomass at relatively low human population density, followed by more gradual declines as human population density increased further. Adjusting for other factors, the highest levels of oceanic productivity among our study locations were associated with more than double the biomass of reef fishes (including ~4 times the biomass of planktivores and piscivores) compared to islands with lowest oceanic productivity. Our results emphasize that coral reef areas do not all have equal ability to sustain large reef fish stocks, and that what is natural varies significantly amongst locations. Comparisons of biomass estimates derived from visual surveys with predicted biomass in the absence of humans indicated that total reef fish biomass was depleted by 61% to 69% at populated islands in the Mariana Archipelago; by 20% to 78% in the Main Hawaiian islands; and by 21% to 56% in American Samoa.

Species richness on coral reefs and the pursuit of convergent global estimates.

Global species richness, whether estimated by taxon, habitat, or ecosystem, is a key biodiversity metric. Yet, despite the global importance of biodiversity and increasing threats to it (e.g., we are no better able to estimate global species richness now than we were six decades ago. Estimates of global species richness remain highly uncertain and are often logically inconsistent. They are also difficult to validate because estimation of global species richness requires extrapolation beyond the number of species known. Given that somewhere between 3% and >96% of species on Earth may remain undiscovered, depending on the methods used and the taxa considered, such extrapolations, especially from small percentages of known species, are likely to be highly uncertain. An alternative approach is to estimate all species, the known and unknown, directly. Using expert taxonomic knowledge of the species already described and named, those already discovered but not yet described and named, and those still awaiting discovery, we estimate there to be 830,000 (95% credible limits: 550,000-1,330,000) multi-cellular species on coral reefs worldwide, excluding fungi. Uncertainty surrounding this estimate and its components were often strongly skewed toward larger values, indicating that many more species on coral reefs is more plausible than many fewer. The uncertainties revealed here should guide future research toward achieving convergence in global species richness estimates for coral reefs and other ecosystems via adaptive learning protocols whereby such estimates can be tested and improved, and their uncertainties reduced, as new knowledge is acquired.

Conservation management options and actions: putative decline of coral cover at Palmyra Atoll, Northern Line Islands, as a case study.

Localised loss of live coral cover at Palmyra Atoll (central Pacific Ocean) has been attributed to increased temperature and/or sedimentation arising from alterations made to the lagoon system. It has been hypothesised that a causeway spanning the lagoon hinders water circulation, resulting in warmer and/or more turbid water flowing towards a site of high coral cover and diversity (Coral Gardens). Analyses of a multi-site and multi-year data set revealed no differences in mean temperature or turbidity values on either side of the causeway and provided no evidence of significantly warmer or more turbid water at Coral Gardens. We conclude that the putative decline in live coral cover cannot be attributed to the presence of the causeway and that proposed management actions involving modification to the causeway cannot achieve the conservation outcomes suggested of them.

Diel variability in seawater pH relates to calcification and benthic community structure on coral reefs.

Community structure and assembly are determined in part by environmental heterogeneity. While reef-building corals respond negatively to warming (i.e. bleaching events) and ocean acidification (OA), the extent of present-day natural variability in pH on shallow reefs and ecological consequences for benthic assemblages is unknown. We documented high resolution temporal patterns in temperature and pH from three reefs in the central Pacific and examined how these data relate to community development and net accretion rates of early successional benthic organisms. These reefs experienced substantial diel fluctuations in temperature (0.78°C) and pH (>0.2) similar to the magnitude of 'warming' and 'acidification' expected over the next century. Where daily pH within the benthic boundary layer failed to exceed pelagic climatological seasonal lows, net accretion was slower and fleshy, non-calcifying benthic organisms dominated space. Thus, key aspects of coral reef ecosystem structure and function are presently related to natural diurnal variability in pH.

GhostNet marine debris survey in the Gulf of Alaska--satellite guidance and aircraft observations.

Marine debris, particularly debris that is composed of lost or abandoned fishing gear, is recognized as a serious threat to marine life, vessels, and coral reefs. The goal of the GhostNet project is the detection of derelict nets at sea through the use of weather and ocean models, drifting buoys and satellite imagery to locate convergent areas where nets are likely to collect, followed by airborne surveys with trained observers and remote sensing instruments to spot individual derelict nets. These components of GhostNet were first tested together in the field during a 14-day marine debris survey of the Gulf of Alaska in July and August 2003. Model, buoy, and satellite data were used in flight planning. A manned aircraft survey with visible and IR cameras and a LIDAR instrument located debris in the targeted locations, including 102 individual pieces of debris of anthropogenic or terrestrial origin.