Corals survive severe bleaching event in refuges related to taxa, colony size, and water depth.

Marine heatwaves are increasing in frequency and duration, threatening tropical reef ecosystems through intensified coral bleaching events. We examined a strikingly variable spatial pattern of bleaching in Moorea, French Polynesia following a heatwave that lasted from November 2018 to July 2019. In July 2019, four months after the onset of bleaching, we surveyed > 5000 individual colonies of the two dominant coral genera, Pocillopora and Acropora, at 10 m and 17 m water depths, at six forereef sites around the island where temperature was measured. We found severe bleaching increased with colony size for both coral genera, but Acropora bleached more severely than Pocillopora overall. Acropora bleached more at 10 m than 17 m, likely due to higher light availability at 10 m compared to 17 m, or greater daily temperature fluctuation at depth. Bleaching in Pocillopora corals did not differ with depth but instead varied with the interaction of colony size and Accumulated Heat Stress (AHS), in that larger colonies (> 30 cm) were more sensitive to AHS than mid-size (10-29 cm) or small colonies (5-9 cm). Our findings provide insight into complex interactions among coral taxa, colony size, and water depth that produce high spatial variation in bleaching and related coral mortality.

Regional differences in fishing behavior determine whether a marine reserve network enhances fishery yield.

A network of marine reserves can enhance yield in depleted fisheries by protecting populations, particularly large, old spawners that supply larvae for interspersed fishing grounds. The ability of marine reserves to enhance sustainable fisheries is much less evident. We report empirical evidence of a marine reserve network improving yield regionally for a sustainable spiny lobster fishery, apparently through the spillover of adult lobsters and behavioral adaptation by the fishing fleet. Results of a Before-After, Control-Impact analysis found catch, effort, and Catch-Per-Unit Effort increased after the establishment of marine reserves in the northern region of the fishery where fishers responded by fishing intensively at reserve borders, but declined in the southern region where they vacated once productive fishing grounds. The adaptation of the northern region of the fishery may have been aided by a history of collaboration between fishers, scientists, and managers, highlighting the value of collaborative research and education programs for preparing fisheries to operate productively within a seascape that includes a large marine reserve network.

Aging of Copper Nanoparticles in the Marine Environment Regulates Toxicity for a Coastal Phytoplankton Species.

Environmental conditions in aquatic ecosystems transform toxic chemicals over time, influencing their bioavailability and toxicity. Using an environmentally relevant methodology, we tested how exposure to seawater for 1-15 weeks influenced the accumulation and toxicity of copper nanoparticles (nano-Cu) in a marine phytoplankton species. Nano-Cu rapidly agglomerated in seawater and then decreased in size due to Cu dissolution. Dissolution rates declined during weeks 1-4 and remained low until 15 weeks, when the large agglomerates that had formed began to rapidly dissolve again. Marine phytoplankton species were exposed for 5-day periods to nano-Cu aged from 1 to 15 weeks at concentrations from 0.01 to 20 ppm. Toxicity to phytoplankton, measured as change in population growth rate, decreased significantly with particle aging from 0 to 4 weeks but increased substantially in the 15-week treatment due apparently to elevated Cu dissolution of reagglomerated particles. Results indicate that the transformation, fate, and toxicity of nano-Cu in marine ecosystems are influenced by a highly dynamic physicochemical aging process.

Coral reef structural complexity loss exposes coastlines to waves.

Coral reefs offer natural coastal protection by attenuating incoming waves. Here we combine unique coral disturbance-recovery observations with hydrodynamic models to quantify how structural complexity dissipates incoming wave energy. We find that if the structural complexity of healthy coral reefs conditions is halved, extreme wave run-up heights that occur once in a 100-years will become 50 times more frequent, threatening reef-backed coastal communities with increased waves, erosion, and flooding.

Size-dependent mortality of corals during marine heatwave erodes recovery capacity of a coral reef.

For many long-lived taxa, such as trees and corals, older, and larger individuals often have the lowest mortality and highest fecundity. However, climate change-driven disturbances such as droughts and heatwaves may fundamentally alter typical size-dependent patterns of mortality and reproduction in these important foundation taxa. Working in Moorea, French Polynesia, we investigated how a marine heatwave in 2019, one of the most intense marine heatwaves at our sites over the past 30 years, drove patterns of coral bleaching and mortality. The marine heatwave drove island-wide mass coral bleaching that killed up to 76% and 65% of the largest individuals of the two dominant coral genera, Pocillopora and Acropora, respectively. Colonies of Pocillopora and Acropora ≥30 cm diameter were ~3.5× and ~1.3×, respectively, more likely to die than colonies <30-cm diameter. Typically, annual mortality in these corals is concentrated on the smallest size classes. Yet, this heatwave dramatically reshaped this pattern, with heat stress disproportionately killing larger coral colonies and equalizing annual mortality rates across the size spectrum. This shift in the size-mortality relationship reduced the overall fecundity of these genera by >60% because big corals are disproportionately important for reproduction on reefs. Additionally, the survivorship of microscopic coral recruits, critical for the recovery of corals following disturbances, declined to 2%, over an order of magnitude lower compared to a year without elevated thermal stress, where 33% of coral recruits survived. While other research has shown that larger corals can bleach more frequently than smaller corals, we show the severe impact this phenomenon can have at the reef-wide scale. As marine heatwaves become more frequent and intense, disproportionate mortality of the largest, most fecund corals and near-complete loss of entire cohorts of newly-settled coral recruits will likely reduce the recovery capacity of these iconic ecosystems.

Juvenile corals underpin coral reef carbonate production after disturbance.

Sea-level rise is predicted to cause major damage to tropical coastlines. While coral reefs can act as natural barriers for ocean waves, their protection hinges on the ability of scleractinian corals to produce enough calcium carbonate (CaCO3 ) to keep up with rising sea levels. As a consequence of intensifying disturbances, coral communities are changing rapidly, potentially reducing community-level CaCO3 production. By combining colony-level physiology and long-term monitoring data, we show that reefs recovering from major disturbances can produce 40% more CaCO3 than currently estimated due to the disproportionate contribution of juvenile corals. However, the buffering effect of highly productive juvenile corals is compromised by recruitment failures, which have been more frequently observed after large-scale, repeated bleaching events. While the size structure of corals can bolster a critical ecological function on reefs, climate change impacts on recruitment may undermine this buffering effect, thus further compromising the persistence of reefs and their provision of important ecosystem services.

Evidence that spillover from Marine Protected Areas benefits the spiny lobster (Panulirus interruptus) fishery in southern California.

Marine Protected Areas (MPAs) are designed to enhance biodiversity and ecosystem services. Some MPAs are also established to benefit fisheries through increased egg and larval production, or the spillover of mobile juveniles and adults. Whether spillover influences fishery landings depend on the population status and movement patterns of target species both inside and outside of MPAs, as well as the status of the fishery and behavior of the fleet. We tested whether an increase in the lobster population inside two newly established MPAs influenced local catch, fishing effort, and catch-per-unit-effort (CPUE) within the sustainable California spiny lobster fishery. We found greater build-up of lobsters within MPAs relative to unprotected areas, and greater increases in fishing effort and total lobster catch, but not CPUE, in fishing zones containing MPAs vs. those without MPAs. Our results show that a 35% reduction in fishing area resulting from MPA designation was compensated for by a 225% increase in total catch after 6-years, thus indicating at a local scale that the trade-off of fishing ground for no-fishing zones benefitted the fishery.

Conventional and nano-copper pesticides are equally toxic to the estuarine amphipod Leptocheirus plumulosus.

Modern nano-engineered pesticides have great promise for agriculture due to their extended, low dose release profiles that are intended to increase effectiveness but reduce environmental harm. Whether nanopesticides, including copper (Cu) formulations, cause reduced levels of toxicity to non-target aquatic organisms is unclear but important to assess. Predicting how aquatic species respond to incidental exposure to Cu-based nanopesticides is challenging because of the expected very low concentrations in the environment, and the two forms of exposure that may occur, namely to Cu ions and Cu nanoparticles. We conducted Cu speciation, tissue uptake, and 7-day toxicity laboratory experiments to test how a model estuarine organism, the amphipod Leptocheirus plumulosus, responded to two popular Cu-based nanopesticides, CuPRO and Kocide, and conventional CuCl2. Exposure concentrations ranged from 0 to 2.5 ppm, which were similar to those found in estuarine water located downstream of agricultural fields. Cu dissolution rates were much slower for the nanopesticides than the ionic formula, and Cu body burden in amphipods increased approximately linearly with the nominal exposure concentration. Amphipod survival declined in a normal dose-response manner with no difference among Cu formulations. Growth and movement rates after 7 days revealed no difference among exposure levels when analyzed with conventional statistical methods. By contrast, analysis of respiration rates, inferred from biomass measurements, with a bioenergetic toxicodynamic model indicated potential for population-level effects of exposure to very low-levels of the two nanopesticides, as well as the control contaminant CuCl2. Our results indicate that toxicity assessment of environmental trace pollutant concentrations may go undetected with traditional ecotoxicological tests. We present a process integrating toxicity test results and toxicodynamic modeling that can improve our capacity to detect and predict environmental impacts of very low levels of nanomaterials released into the environment.

Perceptions and responses of Pacific Island fishers to changing coral reefs.

The transformation of coral reefs has profound implications for millions of people. However, the interactive effects of changing reefs and fishing remain poorly resolved. We combine underwater surveys (271 000 fishes), catch data (18 000 fishes), and household surveys (351 households) to evaluate how reef fishes and fishers in Moorea, French Polynesia responded to a landscape-scale loss of coral caused by sequential disturbances (a crown-of-thorns sea star outbreak followed by a category 4 cyclone). Although local communities were aware of the disturbances, less than 20% of households reported altering what fishes they caught or ate. This contrasts with substantial changes in the taxonomic composition in the catch data that mirrored changes in fish communities observed on the reef. Our findings highlight that resource users and scientists may have very different interpretations of what constitutes 'change' in these highly dynamic social-ecological systems, with broad implications for successful co-management of coral reef fisheries.

Predicting coral community recovery using multi-species population dynamics models.

Predicting whether, how, and to what degree communities recover from disturbance remain major challenges in ecology. To predict recovery of coral communities we applied field survey data of early recovery dynamics to a multi-species integral projection model that captured key demographic processes driving coral population trajectories, notably density-dependent larval recruitment. After testing model predictions against field observations, we updated the model to generate projections of future coral communities. Our results indicated that communities distributed across an island landscape followed different recovery trajectories but would reassemble to pre-disturbed levels of coral abundance, composition, and size, thus demonstrating persistence in the provision of reef habitat and other ecosystem services. Our study indicates that coral community dynamics are predictable when accounting for the interplay between species life-history, environmental conditions, and density-dependence. We provide a quantitative framework for evaluating the ecological processes underlying community trajectory and characteristics important to ecosystem functioning.

Environmental Benefits of Novel Nonhuman Food Inputs to Salmon Feeds.

Global population growth and changing diets increase the importance, and challenges, of reducing the environmental impacts of food production. Farmed seafood is a relatively efficient way to produce protein and has already overtaken wild fisheries. The use of protein-rich food crops, such as soy, instead of fishmeal in aquaculture feed diverts these important protein sources away from direct human consumption and creates new environmental challenges. Single cell proteins (SCPs), including bacteria and yeast, have recently emerged as replacements for plant-based proteins in salmon feeds. Attributional life cycle assessment is used to compare salmon feeds based on protein from soy, methanotrophic bacteria, and yeast ingredients. All ingredients are modeled at the industrial production scale and compared based on seven resource use and emissions indicators. Yeast protein concentrate showed drastically lower impacts in all categories compared to soy protein concentrate. Bacteria meal also had lower impacts than soy protein concentrate for five of the seven indicators. When these target meals were incorporated into complete feeds the relative trends remain fairly constant, but benefits of the novel ingredients are dampened by high impacts from the nontarget ingredients. Particularly, primary production requirements (PPR) are about equal and constant across all feeds for both analyses since PPR was driven by fishmeal and oil. The bacteria-based feed has the highest climate change impacts due to the use of methane to feed the bacteria who then release carbon dioxide. Overall, the results of this study suggest that incorporating SCP ingredients into salmon feeds can help reduce the environmental impacts of salmon production. Continued improvements in SCP production would further increase the sustainability of salmon farming.

Predicting coral community recovery using multi-species population dynamics models.

Predicting whether, how, and to what degree communities recover from disturbance remain major challenges in ecology. To predict recovery of coral communities we applied field survey data of early recovery dynamics to a multi-species integral projection model that captured key demographic processes driving coral population trajectories, notably density-dependent larval recruitment. After testing model predictions against field observations, we updated the model to generate projections of future coral communities. Our results indicated that communities distributed across an island landscape followed different recovery trajectories but would reassemble to pre-disturbed levels of coral abundance, composition, and size, thus demonstrating persistence in the provision of reef habitat and other ecosystem services. Our study indicates that coral community dynamics are predictable when accounting for the interplay between species life-history, environmental conditions, and density-dependence. We provide a quantitative framework for evaluating the ecological processes underlying community trajectory and characteristics important to ecosystem functioning.

Recruitment Drives Spatial Variation in Recovery Rates of Resilient Coral Reefs.

Tropical reefs often undergo acute disturbances that result in landscape-scale loss of coral. Due to increasing threats to coral reefs from climate change and anthropogenic perturbations, it is critical to understand mechanisms that drive recovery of these ecosystems. We explored this issue on the fore reef of Moorea, French Polynesia, following a crown-of-thorns seastar outbreak and cyclone that dramatically reduced cover of coral. During the five-years following the disturbances, the rate of re-establishment of coral cover differed systematically around the triangular-shaped island; coral cover returned most rapidly at sites where the least amount of live coral remained after the disturbances. Although sites differed greatly in the rate of return of coral, all showed at least some evidence of re-assembly to their pre-disturbance community structure in terms of relative abundance of coral taxa and other benthic space holders. The primary driver of spatial variation in recovery was recruitment of sexually-produced corals; subsequent growth and survivorship were less important in shaping the spatial pattern. Our findings suggest that, although the coral community has been resilient, some areas are unlikely to attain the coral cover and taxonomic structure they had prior to the most recent disturbances before the advent of another landscape-scale perturbation.

Photosynthetic efficiency predicts toxic effects of metal nanomaterials in phytoplankton.

High Throughput Screening (HTS) using in vitro assessments at the subcellular level has great promise for screening new chemicals and emerging contaminants to identify high-risk candidates, but their linkage to ecological impacts has seldom been evaluated. We tested whether a battery of subcellular HTS tests could be used to accurately predict population-level effects of engineered metal nanoparticles (ENPs) on marine phytoplankton, important primary producers that support oceanic food webs. To overcome well-known difficulties of estimating ecologically meaningful toxicity parameters, we used novel Dynamic Energy Budget and Toxicodynamic (DEBtox) modeling techniques to evaluate impacts of ENPs on population growth rates. Our results show that population growth was negatively impacted by all four ENPs tested, but the HTS tests assessing many cell/physiological functions lacked predictive power at the population level. However, declining photosynthetic efficiency, a traditional physiological endpoint for photoautotrophs, was a good predictor of population level effects in phytoplankton. DEBtox techniques provided robust estimates of EC10 for population growth rates in exponentially growing batch cultures of phytoplankton, and should be widely useful for ecotoxicological testing. Adoption of HTS approaches for ecotoxicological assessment should carefully evaluate the predictive power of specific assays to minimize the risk that effects at higher levels of biological organization may go undetected.

Considerations of Environmentally Relevant Test Conditions for Improved Evaluation of Ecological Hazards of Engineered Nanomaterials.

Engineered nanomaterials (ENMs) are increasingly entering the environment with uncertain consequences including potential ecological effects. Various research communities view differently whether ecotoxicological testing of ENMs should be conducted using environmentally relevant concentrations-where observing outcomes is difficult-versus higher ENM doses, where responses are observable. What exposure conditions are typically used in assessing ENM hazards to populations? What conditions are used to test ecosystem-scale hazards? What is known regarding actual ENMs in the environment, via measurements or modeling simulations? How should exposure conditions, ENM transformation, dose, and body burden be used in interpreting biological and computational findings for assessing risks? These questions were addressed in the context of this critical review. As a result, three main recommendations emerged. First, researchers should improve ecotoxicology of ENMs by choosing test end points, duration, and study conditions-including ENM test concentrations-that align with realistic exposure scenarios. Second, testing should proceed via tiers with iterative feedback that informs experiments at other levels of biological organization. Finally, environmental realism in ENM hazard assessments should involve greater coordination among ENM quantitative analysts, exposure modelers, and ecotoxicologists, across government, industry, and academia.

Simulating social-ecological systems: the Island Digital Ecosystem Avatars (IDEA) consortium.

Systems biology promises to revolutionize medicine, yet human wellbeing is also inherently linked to healthy societies and environments (sustainability). The IDEA Consortium is a systems ecology open science initiative to conduct the basic scientific research needed to build use-oriented simulations (avatars) of entire social-ecological systems. Islands are the most scientifically tractable places for these studies and we begin with one of the best known: Moorea, French Polynesia. The Moorea IDEA will be a sustainability simulator modeling links and feedbacks between climate, environment, biodiversity, and human activities across a coupled marine-terrestrial landscape. As a model system, the resulting knowledge and tools will improve our ability to predict human and natural change on Moorea and elsewhere at scales relevant to management/conservation actions.

Fishing diseased abalone to promote yield and conservation.

Past theoretical models suggest fishing disease-impacted stocks can reduce parasite transmission, but this is a good management strategy only when the exploitation required to reduce transmission does not overfish the stock. We applied this concept to a red abalone fishery so impacted by an infectious disease (withering syndrome) that stock densities plummeted and managers closed the fishery. In addition to the non-selective fishing strategy considered by past disease-fishing models, we modelled targeting (culling) infected individuals, which is plausible in red abalone because modern diagnostic tools can determine infection without harming landed abalone and the diagnostic cost is minor relative to the catch value. The non-selective abalone fishing required to eradicate parasites exceeded thresholds for abalone sustainability, but targeting infected abalone allowed the fishery to generate yield and reduce parasite prevalence while maintaining stock densities at or above the densities attainable if the population was closed to fishing. The effect was strong enough that stock and yield increased even when the catch was one-third uninfected abalone. These results could apply to other fisheries as the diagnostic costs decline relative to catch value.

Impacts of Silver Nanoparticles on a Natural Estuarine Plankton Community.

Potential effects of metal nanoparticles on aquatic organisms and food webs are hard to predict from the results of single-species tests under controlled laboratory conditions, and more realistic exposure experiments are rarely conducted. We tested whether silver nanoparticles (Ag NPs) had an impact on zooplankton grazing on their prey, specifically phytoplankton and bacterioplankton populations. If Ag NPs directly reduced the abundance of prey, thereby causing the overall rate of grazing by their predators to decrease, a cascading effect on a planktonic estuarine food web would be seen. Our results show that the growth rates of both phytoplankton and bacterioplankton populations were significantly reduced by Ag NPs at concentrations of ≥500 µg L(-1). At the same time, grazing rates on these populations tended to decline with exposure to Ag NPs. Therefore, Ag NPs did not cause a cascade of effects through the food web but impacted a specific trophic level. Photosynthetic efficiency of the phytoplankton was significantly reduced at Ag NPs concentrations of ≥500 µg L(-1). These effects did not occur at relatively low concentrations of Ag that are often toxic to single species of bacteria and other organisms, suggesting that the impacts of Ag NP exposure may not be apparent at environmentally relevant concentrations due to compensatory processes at the community level.

Species sensitivity distributions for engineered nanomaterials.

Engineered nanomaterials (ENMs) are a relatively new strain of materials for which little is understood about their impacts. A species sensitivity distribution (SSDs) is a cumulative probability distribution of a chemical's toxicity measurements obtained from single-species bioassays of various species that can be used to estimate the ecotoxicological impacts of a chemical. The recent increase in the availability of acute toxicity data for ENMs enabled the construction of 10 ENM-specific SSDs, with which we analyzed (1) the range of toxic concentrations, (2) whether ENMs cause greater hazard to an ecosystem than the ionic or bulk form, and (3) the key parameters that affect variability in toxicity. The resulting estimates for hazardous concentrations at which 5% of species will be harmed ranged from <1 ug/L for PVP-coated n-Ag to >3.5 mg/L for CNTs. The results indicated that size, formulation, and the presence of a coating can alter toxicity, and thereby corresponding SSDs. Few statistical differences were observed between SSDs of an ENM and its ionic counterpart. However, we did find a significant correlation between the solubility of ENMs and corresponding SSD. Uncertainty in SSD values can be reduced through greater consideration of ENM characteristics and physiochemical transformations in the environment.

Cellular partitioning of nanoparticulate versus dissolved metals in marine phytoplankton.

Discharges of metal oxide nanoparticles into aquatic environments are increasing with their use in society, thereby increasing exposure risk for aquatic organisms. Separating the impacts of nanoparticle from dissolved metal pollution is critical for assessing the environmental risks of the rapidly growing nanomaterial industry, especially in terms of ecosystem effects. Metal oxides negatively affect several species of marine phytoplankton, which are responsible for most marine primary production. Whether such toxicity is generally due to nanoparticles or exposure to dissolved metals liberated from particles is uncertain. The type and severity of toxicity depends in part on whether phytoplankton cells take up and accumulate primarily nanoparticles or dissolved metal ions. We compared the responses of the marine diatom, Thalassiosira weissflogii, exposed to ZnO, AgO, and CuO nanoparticles with the responses of T. weissflogii cells exposed to the dissolved metals ZnCl2, AgNO3, and CuCl2 for 7 d. Cellular metal accumulation, metal distribution, and algal population growth were measured to elucidate differences in exposure to the different forms of metal. Concentration-dependent metal accumulation and reduced population growth were observed in T. weissflogii exposed to nanometal oxides, as well as dissolved metals. Significant effects on population growth were observed at the lowest concentrations tested for all metals, with similar toxicity for both dissolved and nanoparticulate metals. Cellular metal distribution, however, markedly differed between T. weissflogii exposed to nanometal oxides versus those exposed to dissolved metals. Metal concentrations were highest in the algal cell wall when cells were exposed to metal oxide nanoparticles, whereas algae exposed to dissolved metals had higher proportions of metal in the organelle and endoplasmic reticulum fractions. These results have implications for marine plankton communities as well as higher trophic levels, since metal may be transferred from phytoplankton through food webs vis à vis grazing by zooplankton or other pathways.