Hunter S. Lenihan

A Global Map of Human Impact on Marine Ecosystems

The management and conservation of the worlds oceans require synthesis of spatial data on the distribution and intensity of human activities and the overlap of their impacts on marine ecosystems. We developed an ecosystem-specific, multiscale spatial model to synthesize 17 global data sets of anthropogenic drivers of ecological change for 20 marine ecosystems. Our analysis indicates that no area is unaffected by human influence and that a large fraction (41%) is strongly affected by multiple drivers. However, large areas of relatively little human impact remain, particularly near the poles. The analytical process and resulting maps provide flexible tools for regional and global efforts to allocate conservation resources; to implement ecosystem-based management; and to inform marine spatial planning, education, and basic research.

Depletion, degradation, and recovery potential of estuaries and coastal seas.

Estuarine and coastal transformation is as old as civilization yet has dramatically accelerated over the past 150 to 300 years. Reconstructed time lines, causes, and consequences of change in 12 once diverse and productive estuaries and coastal seas worldwide show similar patterns: Human impacts have depleted >90% of formerly important species, destroyed >65% of seagrass and wetland habitat, degraded water quality, and accelerated species invasions. Twentieth-century conservation efforts achieved partial recovery of upper trophic levels but have so far failed to restore former ecosystem structure and function. Our results provide detailed historical baselines and quantitative targets for ecosystem-based management and marine conservation.

Stability and Aggregation of Metal Oxide Nanoparticles in Natural Aqueous Matrices

There is a pressing need for information on the mobility of nanoparticles in the complex aqueous matrices found in realistic environmental conditions. We dispersed three different metal oxide nanoparticles (TiO(2), ZnO and CeO(2)) in samples taken from eight different aqueous media associated with seawater, lagoon, river, and groundwater, and measured their electrophoretic mobility, state of aggregation, and rate of sedimentation. The electrophoretic mobility of the particles in a given aqueous media was dominated by the presence of natural organic matter (NOM) and ionic strength, and independent of pH. NOM adsorbed onto these nanoparticles significantly reduces their aggregation, stabilizing them under many conditions. The transition from reaction to diffusion limited aggregation occurs at an electrophoretic mobility from around -2 to -0.8 microm s(-1) V(-1) cm. These results are key for designing and interpreting nanoparticle ecotoxicity studies in various environmental conditions.

Oyster Reefs at Risk and Recommendations for Conservation, Restoration, and Management

Native oyster reefs once dominated many estuaries, ecologically and economically. Centuries of resource extraction exacerbated by coastal degradation have pushed oyster reefs to the brink of functional extinction worldwide. We examined the condition of oyster reefs across 144 bays and 44 ecoregions; our comparisons of past with present abundances indicate that more than 90% of them have been lost in bays (70%) and ecoregions (63%). In many bays, more than 99% of oyster reefs have been lost and are functionally extinct. Overall, we estimate that 85% of oyster reefs have been lost globally. Most of the worlds remaining wild capture of native oysters (> 75%) comes from just five ecoregions in North America, yet the condition of reefs in these ecoregions is poor at best, except in the Gulf of Mexico. We identify many cost-effective solutions for conservation, restoration, and the management of fisheries and nonnative species that could reverse these oyster losses and restore reef ecosystem services.

HOW HABITAT DEGRADATION THROUGH FISHERY DISTURBANCE ENHANCES IMPACTS OF HYPOXIA ON OYSTER REEFS

Oysters are ecosystem engineers that create biogenic reef habitat important to estuarine biodiversity, benthic-pelagic coupling, and fishery production. Prevailing ex- planations for the dramatic decline of eastern oysters (Crassostrea virginica) during the last century overlook ecosystem complexity by ignoring interactions among multiple en- vironmental disturbances. To explain oyster loss, we tested whether (1) mortality of oysters on natural oyster reefs varies with water depth (3 m vs. 6 m), (2) harvesting by oyster dredges reduces the height of oyster reefs, and (3) bottom-water hypoxia/anoxia and re- duction in reef height through fishery disturbance interact to enhance mortality of oysters in the Neuse River estuary, North Carolina, USA. The percentage of oysters found dead (mean ? 1 SD) during a survey of natural reefs in May 1993 was significantly greater at 6-m (92 ? 10%) than at 3-m (28 ? 9%) water depth. Less than one seasons worth of oyster dredging reduced the height of restored oyster reefs by -30%. During stratification of the water column in summer, oxygen depletion near the seafloor at 6 m caused mass mortality of oysters, other invertebrates, and fishes on short, deep experimental reefs, while oysters and other reef associates elevated into the surface layer by sufficient reef height or by location in shallow water survived. Highly mobile blue crabs (Callinectes sapidus) abandoned burrows located in hypoxic/anoxic bottom waters but remained alive in shallow water. Our results indicate that interaction of reef habitat degradation (height reduction) through fishery disturbance and extended bottom-water hypoxia/anoxia caused the pattern of oyster mortality observed on natural reefs and influences the abundance and distribution of fish and invertebrate species that utilize this temperate reef habitat. Interactions among environmental disturbances imply a need for the integrative approaches of ecosystem man- agement to restore and sustain estuarine habitat.

PHYSICAL-BIOLOGICAL COUPLING ON OYSTER REEFS: HOW HABITAT STRUCTURE INFLUENCES INDIVIDUAL PERFORMANCE

A large-scale field experiment was conducted to test whether the physical structure of biogenic reef habitat controls physical conditions (hydrodynamics and hydro- graphics) with subsequent influence on the performance (recruitment, growth, and survival) of a benthic suspension feeder. The experimental system consisted of restored subtidal oyster reefs inhabited by the eastern oyster Crassostrea virginica. To determine whether the size of reefs influences the flow environment and oyster performance, reefs of four heights-tall (2 m), short (1 m), dredged (0.6 m), and low (0.1 m)-were constructed at 3-m water depth in the Neuse River estuary, North Carolina, USA. To test whether oyster performance varies with water depth and hydrographic conditions, tall and short reefs were also constructed at 6-m water depth. Flow speed, sedimentation, temperature, salinity, dissolved oxygen, and the performance of oysters were measured as a function of reef height, position on reef, and water depth over a 10-mo period. Flow speed was found to increase on reefs with reef height and elevation on reefs. Rates of sediment deposition were seasonally highest where flow speed was lowest, at the bases of reefs, and seasonally decreased with increasing water depth. More than 90% of the surface area of low reefs was buried after only 16 mo of exposure in the estuary, indicating that reef height controls habitat quality (and quantity) indirectly through its effect on flow. Short reefs and the bases of tall reefs at 6-m depth were exposed to a total of 26 d of hypoxia/anoxia. No other reef treatment was exposed to >5 d of hypoxia. Physical conditions on experimental reefs had a profound influence on the performance of oysters as the flow environment alone explained 81 % of variability in oyster growth and mortality. Recruitment of oysters over a 2-mo period was slightly higher on the front bases than the crests of reefs, but did not vary with reef height or water depth. After 10 mo, the shell growth and condition index of genetically similar, hatchery-raised oysters were greatest on the crests of tall and short reefs, where flow speed and quality of suspended food material were highest, and sediment deposition was lowest. Growth was greatest overall at the crests of tall reefs located at 6-m water depth where flow speed was high, and the numbers of days exposed to hypoxia/anoxia and variation in salinity were lowest. Total percentage mortality of oysters after 10 mo was greater on low reefs located at 3-m depth than on all other reef types and was greater on the bases than crests of tall, short, and dredged reefs. Predation by crabs and fishes accounted for 4-20% of total oyster mortality and showed no pattern across reef treatments. Results of this experiment indicate (1) that the physical structure and location of biogenic habitat controls local physical variables and (2) that, in turn, physical variables, especially flow speed, have a profound influence on the performance of a resident species. Realization that an ecological function of habitat is to indirectly control local population production through physical-biological coupling should improve our ability to conserve, restore, and manage habitat and associated species diversity. Better ecological engineering of restored oyster reef habitat is likely to improve fishery production and help maintain estuarine biodiversity.

Cascading of habitat degradation: Oyster reefs invaded by refugee fishes escaping stress

Mobile consumers have potential to cause a cascading of habitat degradation beyond the region that is directly stressed, by concentrating in refuges where they intensify biological interactions and can deplete prey resources. We tested this hypothesis on structurally complex, species-rich biogenic reefs created by the eastern oyster, Crassostrea virginica, in the Neuse River estuary, North Carolina, USA. We (1) sampled fishes and invertebrates on natural and restored reefs and on sand bottom to compare fish utilization of these different habitats and to characterize the trophic relations among large reef-associated fishes and benthic invertebrates, and (2) tested whether bottom-water hypoxia and fishery-caused degradation of reef habitat combine to induce mass emigration of fish that then modify community composition in refuges across an estuarine seascape. Experimentally restored oyster reefs of two heights (1 m tall “degraded” or 2 m tall “natural” reefs) were constructed at 3 and 6 m depths. We sampled...

Impacts of Metal Oxide Nanoparticles on Marine Phytoplankton

Information on the toxicity of environmentally relevant concentrations of nanoparticles in marine ecosystems is needed for informed regulation of these emerging materials. We tested the effects of two types of metal oxide nanoparticles, TiO(2) and ZnO, on population growth rates of four species of marine phytoplankton representing three major coastal groups (diatoms, chlorophytes, and prymnesiophytes). These metal oxide nanoparticles (NPs) are becoming common components in many industrial, household, and cosmetic products that are released into coastal ecosystems. Titania NPs showed no measurable effect on growth rates of any species, while ZnO NPs significantly depressed growth rate of all four species. ZnO NPs aggregated rapidly in seawater, forming particles >400 nm hydrodynamic diameter within 30 min, and dissolved quickly, reaching equilibrium concentrations within 12 h. Toxicity of ZnO NPs to phytoplankton was likely due to dissolution, release, and uptake of free zinc ions, but specific nanoparticulate effects may be difficult to disentangle from effects due to free zinc ions. A modeling approach based on a Dynamic Energy Budget (DEB) framework was used to estimate sublethal effects of the two NPs on phytoplankton populations. Concentrations that were estimated to have no effect on population growth (NEC) were (one standard error in parentheses) 428 (58) μg L(-1) ZnO for the diatom Skeletonema marinoi and 223 (56) μg L(-1) for Thalassiosira pseudonana. NEC could not be estimated for the other taxa but were within the range of 500-1000 μg L(-1). Our results suggest that effects of metal oxide NPs on marine organisms is likely to vary with particle type and organism taxonomy.

TiO2 Nanoparticles Are Phototoxic to Marine Phytoplankton

Nanoparticulate titanium dioxide (TiO2) is highly photoactive, and its function as a photocatalyst drives much of the application demand for TiO2. Because TiO2 generates reactive oxygen species (ROS) when exposed to ultraviolet radiation (UVR), nanoparticulate TiO2 has been used in antibacterial coatings and wastewater disinfection, and has been investigated as an anti-cancer agent. Oxidative stress mediated by photoactive TiO2 is the likely mechanism of its toxicity, and experiments demonstrating cytotoxicity of TiO2 have used exposure to strong artificial sources of ultraviolet radiation (UVR). In vivo tests of TiO2 toxicity with aquatic organisms have typically shown low toxicity, and results across studies have been variable. No work has demonstrated that photoactivity causes environmental toxicity of TiO2 under natural levels of UVR. Here we show that relatively low levels of ultraviolet light, consistent with those found in nature, can induce toxicity of TiO2 nanoparticles to marine phytoplankton, the most important primary producers on Earth. No effect of TiO2 on phytoplankton was found in treatments where UV light was blocked. Under low intensity UVR, ROS in seawater increased with increasing nano-TiO2 concentration. These increases may lead to increased overall oxidative stress in seawater contaminated by TiO2, and cause decreased resiliency of marine ecosystems. Phototoxicity must be considered when evaluating environmental impacts of nanomaterials, many of which are photoactive.

PREDATION STRUCTURES COMMUNITIES AT DEEP-SEA HYDROTHERMAL VENTS

The structure and dynamics of natural communities result from the interplay of abiotic and biotic factors. We used manipulative field experiments to determine the relative roles of abiotic conditions and biotic interactions in structuring deep-sea (2500 m depth) communities along environmental gradients around hydrothermal vents of the eastern tropical Pacific Ocean (East Pacific Rise, at 9 50 N). We tested (1) whether predation by crabs and fishes affects the recruitment of benthic species and subsequent community structure and (2) whether the effects of predation vary along the steep gradients of tem- perature, oxygen, sulfide, and metal concentrations near vents. Recruitment substrates (ba- salt cubic blocks, roughly 10 cm on a side), both uncaged and caged to exclude predators (crabs, fishes, whelks, and octopi), were deployed along a decreasing vent fluid-flux gra- dient. The exclusion of predators for 8 mo increased the abundance of small mobile gas- tropods and amphipod crustaceans but decreased the abundance of sessile invertebrates, including juvenile vestimentiferan worms, tubiculous polychaetes, and mussels. Effects of predation were strongest nearest to hydrothermal vents, where abiotic environmental con- ditions were most extreme but productivity and the overall abundances of benthic inver- tebrates and mobile predators were the greatest. Additional 5-mo experiments conducted at three different locations showed similar trends at all sites, indicating that these effects of predation on benthic community structure are repeatable. Stomach-content analyses of the most abundant predators found at vents indicated that the zoarcid fish ( Thermarces cerberus) primarily feeds on the vent snail Cyathermia naticoides, the limpet Lepetodrilus elevatus, and the amphipod crustacean Ventiella sulfuris, the very species that showed the greatest increase following predator exclusion. In contrast, brachyuran ( Bythograea ther- mydron) and galatheid (Munidopsis subsquamosa ) crab stomachs did not contain small mobile grazers, and crabs presented with arrays of the most common vent invertebrate species preferred mussels and vestimentiferans over limpets. Our results indicate that pre- dation by large mobile predators influences the structure of hydrothermal vent communities, directly by reducing the abundance of gastropod prey species, and indirectly by reducing