Effects of seagrass restoration on coastal fish abundance and diversity.

Restoration is accelerating to reverse global declines of key habitats and recover lost ecosystem functions, particularly in coastal ecosystems. However, there is high uncertainty about the long-term capacity of restored ecosystems to provide habitat and increase biodiversity and the degree to which these ecosystem services are mediated by spatial and temporal environmental variability. We addressed these gaps by sampling fishes biannually for 5-7 years (2012-2018) at 16 sites inside and outside a rapidly expanding restored seagrass meadow in coastal Virginia (USA). Despite substantial among-year variation in abundance and species composition, seine catches in restored seagrass beds were consistently larger (6.4 times more fish, p < 0.001) and more speciose (2.6 times greater species richness, p < 0.001; 3.1 times greater Hill-Shannon diversity, p = 0.03) than seine catches in adjacent unvegetated areas. Catches were particularly larger during summer than autumn (p < 0.01). Structural equation modeling revealed that depth and water residence time interacted to control seagrass presence, leading to higher fish abundance and richness in shallow, well-flushed areas that supported seagrass. Together, our results indicate that seagrass restoration yields large and consistent benefits for many coastal fishes, but that restoration and its benefits are sensitive to the dynamic seascapes in which restoration is conducted. Consideration of how seascape-scale environmental variability affects the success of habitat restoration and subsequent ecosystem function will improve restoration outcomes and the provisioning of ecosystem services.

Efectos de la restauración de pastos marinos sobre la abundancia y diversidad de peces costeros Resumen La restauración ecológica está acelerándose para revertir la declinación mundial de hábitats importantes y para recuperar las funciones ambientales perdidas, particularmente en los ecosistemas costeros. Sin embargo, hay una gran incertidumbre en cuanto a la capacidad a largo plazo que tienen los ecosistemas restaurados de proporcionar hábitats e incrementar la biodiversidad y el grado al que estos servicios ambientales están mediados por la variabilidad ambiental espacial y temporal. Abordamos estos vacíos mediante el muestreo bianual de peces durante 5-7 años (2012-2018) en 16 sitios dentro y fuera de una pradera restaurada de pastos marinos con expansión acelerada en la costa de Virginia (E.U.A.). A pesar de la variación sustancial anual en abundancia y composición de especies, la captura de cerco en los lechos de pastos marinos restaurados fue mayor (6.4 veces más peces, p< 0.001) y con más especies (2.6 veces mayor riqueza de especies, p< 0.001; 3.1 veces mayor diversidad Hill-Shannon, p= 0.03) que la captura de cerco en las áreas aledañas sin vegetación. En particular, las capturas fueron mayores durante el verano que durante el otoño (p < 0.01). Los modelos de ecuaciones estructurales revelaron que la profundidad y el tiempo de residencia acuática interactúan para controlar la presencia de los pastos marinos, lo que resulta en una mayor abundancia y riqueza de peces en áreas someras con buena circulación que fomentan los pastos marinos. En conjunto, nuestros resultados indican que la restauración de los pastos marinos produce grandes beneficios constantes para muchos peces costeros, pero también que la restauración y sus beneficios son sensibles a la dinámica marina en la que se realiza la restauración. Si se considera cómo la variabilidad ambiental a escala de paisaje afecta el éxito de la restauración del hábitat y la función ambiental subsecuente, entonces mejorarán los resultados de restauración y el suministro de servicios ambientales.

The greenhouse gas offset potential from seagrass restoration.

Awarding CO2 offset credits may incentivize seagrass restoration projects and help reverse greenhouse gas (GHG) emissions from global seagrass loss. However, no study has quantified net GHG removal from the atmosphere from a seagrass restoration project, which would require coupled Corg stock and GHG flux enhancement measurements, or determined whether the creditable offset benefit can finance the restoration. We measured all of the necessary GHG accounting parameters in the 7-km2 Zostera marina (eelgrass) meadow in Virginia, U.S.A., part of the largest, most cost-effective meadow restoration to date, to provide the first seagrass offset finance test-of-concept. Restoring seagrass removed 9,600 tCO2 from the atmosphere over 15 years but also enhanced both CH4 and N2O production, releasing 950 tCO2e. Despite tripling the N2O flux to 0.06 g m-2 yr-1 and increasing CH4 8-fold to 0.8 g m-2 yr-1, the meadow now offsets 0.42 tCO2e ha-1 yr-1, which is roughly equivalent to the seagrass sequestration rate for GHG inventory accounting but lower than the rates for temperate and tropical forests. The financial benefit for this highly successful project, $87 K at $10 MtCO2e-1, defrays ~10% of the restoration cost. Managers should also consider seagrass co-benefits, which provide additional incentives for seagrass restoration.

Author Correction: The future of Blue Carbon science.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

The future of Blue Carbon science.

The term Blue Carbon (BC) was first coined a decade ago to describe the disproportionately large contribution of coastal vegetated ecosystems to global carbon sequestration. The role of BC in climate change mitigation and adaptation has now reached international prominence. To help prioritise future research, we assembled leading experts in the field to agree upon the top-ten pending questions in BC science. Understanding how climate change affects carbon accumulation in mature BC ecosystems and during their restoration was a high priority. Controversial questions included the role of carbonate and macroalgae in BC cycling, and the degree to which greenhouse gases are released following disturbance of BC ecosystems. Scientists seek improved precision of the extent of BC ecosystems; techniques to determine BC provenance; understanding of the factors that influence sequestration in BC ecosystems, with the corresponding value of BC; and the management actions that are effective in enhancing this value. Overall this overview provides a comprehensive road map for the coming decades on future research in BC science.

Seagrass blue carbon spatial patterns at the meadow-scale.

Most information on seagrass carbon burial derives from point measurements, which are sometimes scaled by meadow area to estimate carbon stocks; however, sediment organic carbon (Corg) concentrations may vary with distance from the meadow edge, resulting in spatial gradients that affect the accuracy of stock estimates. We mapped sediment Corg concentrations throughout a large (6 km2) restored seagrass meadow to determine whether Corg distribution patterns exist at different spatial scales. The meadow originated from ≤1-acre plots seeded between 2001 and 2004, so we expected Corg to vary spatially according to the known meadow age at sample sites and with proximity to the meadow edge. Applying spatial autoregressive models allowed us to control for spatial autocorrelation and quantify the relative effects of edge proximity and age on Corg concentrations. We found that edge proximity, not age, significantly predicted the meadow-scale Corg distribution. We also evaluated relationships between Corg and a variety of specific explanatory variables, including site relative exposure, shoot density, sediment grain size, and bathymetry. Factors known to affect carbon burial at the plot-scale, such as meadow age and shoot density, were not significant controls on the meadow-scale Corg distribution. Strong correlations between Corg, grain size, and edge proximity suggest that current attenuation increases fine-sediment deposition and, therefore, carbon burial with distance into the meadow. By mapping the sediment Corg pool, we provide the first accurate quantification of an enhanced carbon stock attributable to seagrass restoration. The top 12 cm of the bed contain 3660 t Corg, approximately 1200 t more Corg than an equal area of bare sediment. Most of that net increase is concentrated in a meadow area with low tidal current velocities. Managers should account for the effects of meadow configuration and current velocity when estimating seagrass blue carbon stocks. Our results suggest that a large, contiguous meadow should store more blue carbon than an equal area of small meadow patches.

Seagrass restoration enhances "blue carbon" sequestration in coastal waters.

Seagrass meadows are highly productive habitats that provide important ecosystem services in the coastal zone, including carbon and nutrient sequestration. Organic carbon in seagrass sediment, known as "blue carbon," accumulates from both in situ production and sedimentation of particulate carbon from the water column. Using a large-scale restoration (>1700 ha) in the Virginia coastal bays as a model system, we evaluated the role of seagrass, Zosteramarina, restoration in carbon storage in sediments of shallow coastal ecosystems. Sediments of replicate seagrass meadows representing different age treatments (as time since seeding: 0, 4, and 10 years), were analyzed for % carbon, % nitrogen, bulk density, organic matter content, and ²¹°Pb for dating at 1-cm increments to a depth of 10 cm. Sediment nutrient and organic content, and carbon accumulation rates were higher in 10-year seagrass meadows relative to 4-year and bare sediment. These differences were consistent with higher shoot density in the older meadow. Carbon accumulation rates determined for the 10-year restored seagrass meadows were 36.68 g C m⁻² yr⁻¹. Within 12 years of seeding, the restored seagrass meadows are expected to accumulate carbon at a rate that is comparable to measured ranges in natural seagrass meadows. This the first study to provide evidence of the potential of seagrass habitat restoration to enhance carbon sequestration in the coastal zone.

Genetic diversity enhances restoration success by augmenting ecosystem services.

Disturbance and habitat destruction due to human activities is a pervasive problem in near-shore marine ecosystems, and restoration is often used to mitigate losses. A common metric used to evaluate the success of restoration is the return of ecosystem services. Previous research has shown that biodiversity, including genetic diversity, is positively associated with the provision of ecosystem services. We conducted a restoration experiment using sources, techniques, and sites similar to actual large-scale seagrass restoration projects and demonstrated that a small increase in genetic diversity enhanced ecosystem services (invertebrate habitat, increased primary productivity, and nutrient retention). In our experiment, plots with elevated genetic diversity had plants that survived longer, increased in density more quickly, and provided more ecosystem services (invertebrate habitat, increased primary productivity, and nutrient retention). We used the number of alleles per locus as a measure of genetic diversity, which, unlike clonal diversity used in earlier research, can be applied to any organism. Additionally, unlike previous studies where positive impacts of diversity occurred only after a large disturbance, this study assessed the importance of diversity in response to potential environmental stresses (high temperature, low light) along a water-depth gradient. We found a positive impact of diversity along the entire depth gradient. Taken together, these results suggest that ecosystem restoration will significantly benefit from obtaining sources (transplants or seeds) with high genetic diversity and from restoration techniques that can maintain that genetic diversity.

A meta-analysis of seaweed impacts on seagrasses: generalities and knowledge gaps.

Seagrasses are important habitat-formers and ecosystem engineers that are under threat from bloom-forming seaweeds. These seaweeds have been suggested to outcompete the seagrasses, particularly when facilitated by eutrophication, causing regime shifts where green meadows and clear waters are replaced with unstable sediments, turbid waters, hypoxia, and poor habitat conditions for fishes and invertebrates. Understanding the situations under which seaweeds impact seagrasses on local patch scales can help proactive management and prevent losses at greater scales. Here, we provide a quantitative review of available published manipulative experiments (all conducted at the patch-scale), to test which attributes of seaweeds and seagrasses (e.g., their abundances, sizes, morphology, taxonomy, attachment type, or origin) influence impacts. Weighted and unweighted meta-analyses (Hedges d metric) of 59 experiments showed generally high variability in attribute-impact relationships. Our main significant findings were that (a) abundant seaweeds had stronger negative impacts on seagrasses than sparse seaweeds, (b) unattached and epiphytic seaweeds had stronger impacts than 'rooted' seaweeds, and (c) small seagrass species were more susceptible than larger species. Findings (a) and (c) were rather intuitive. It was more surprising that 'rooted' seaweeds had comparatively small impacts, particularly given that this category included the infamous invasive Caulerpa species. This result may reflect that seaweed biomass and/or shading and metabolic by-products like anoxia and sulphides could be lower for rooted seaweeds. In conclusion, our results represent simple and robust first-order generalities about seaweed impacts on seagrasses. This review also documented a limited number of primary studies. We therefore identified major knowledge gaps that need to be addressed before general predictive models on seaweed-seagrass interactions can be build, in order to effectively protect seagrass habitats from detrimental competition from seaweeds.

GRACILARIA VERMICULOPHYLLA (RHODOPHYTA, GRACILARIALES) IN THE VIRGINIA COASTAL BAYS, USA: COX1 ANALYSIS REVEALS HIGH GENETIC RICHNESS OF AN INTRODUCED MACROALGA.

Gracilaria vermiculophylla (Ohmi) Papenfuss is an invasive alga that is native to Southeast Asia and has invaded many estuaries in North America and Europe. It is difficult to differentiate G. vermiculophylla from native forms using morphology and therefore molecular techniques are needed. In this study, we used three molecular markers (rbcL, cox2-cox3 spacer, cox1) to identify G. vermiculophylla at several locations in the western Atlantic. RbcL and cox2-cox3 spacer markers confirmed the presence of G. vermiculophylla on the east coast of the USA from Massachusetts to South Carolina. We used a 507 base pair region of cox1 mtDNA to (i) verify the widespread distribution of G. vermiculophylla in the Virginia (VA) coastal bays and (ii) determine the intraspecific diversity of these algae. Cox1 haplotype richness in the VA coastal bays was much higher than that previously found in other invaded locations, as well as some native locations. This difference is likely attributed to the more intensive sampling design used in this study, which was able to detect richness created by multiple, diverse introductions. On the basis of our results, we recommend that future studies take differences in sampling design into account when comparing haplotype richness and diversity between native and non-native studies in the literature.

Habitat cascades: the conceptual context and global relevance of facilitation cascades via habitat formation and modification.

The importance of positive interactions is increasingly acknowledged in contemporary ecology. Most research has focused on direct positive effects of one species on another. However, there is recent evidence that indirect positive effects in the form of facilitation cascades can also structure species abundances and biodiversity. Here we conceptualize a specific type of facilitation cascade-the habitat cascade. The habitat cascade is defined as indirect positive effects on focal organisms mediated by successive facilitation in the form of biogenic formation or modification of habitat. Based on a literature review, we demonstrate that habitat cascades are a general phenomenon that enhances species abundance and diversity in forests, salt marshes, seagrass meadows, and seaweed beds. Habitat cascades are characterized by a hierarchy of facilitative interactions in which a basal habitat former (typically a large primary producer, e.g., a tree) creates living space for an intermediate habitat former (e.g., an epiphyte) that in turn creates living space for the focal organisms (e.g., spiders, beetles, and mites). We then present new data on a habitat cascade common to soft-bottom estuaries in which a relatively small invertebrate provides basal habitat for larger intermediate seaweeds that, in turn, generate habitat for focal invertebrates and epiphytes. We propose that indirect positive effects on focal organisms will be strongest when the intermediate habitat former is larger and different in form and function from the basal habitat former. We also discuss how humans create, modify, and destroy habitat cascades via global habitat destruction, climatic change, over-harvesting, pollution, or transfer of invasive species. Finally, we outline future directions for research that will lead to a better understanding of habitat cascades.

Nitrogen fixation and nitrogen limitation of primary production along a natural marsh chronosequence.

Nitrogen (N) limitation of primary production is common in temperate salt marshes, even though conservative N recycling can fulfill a large proportion of plant N demand. In nutrient poor young marshes, N limitation may be more severe and new N sources, such as N fixation, more important for plant growth. We measured N fixation and the response of salt marsh primary producers (Spartina alterniflora and benthic microalgae) to N fertilization in one mature (>150 year) and two young (7 and 15 year) naturally developing marshes at the Virginia Coast Reserve LTER site. S. alterniflora aboveground biomass in the mature marsh (1,700+/-273 g m(-2)) was 1.8 and 2.8 times higher than in the 15 year and 7 year old marshes, respectively. Fertilization significantly increased S. alterniflora biomass in the two young marshes (160-175%) and areal aboveground tissue N in the youngest marsh (260%). Microalgal chlorophyll a (Chl a) in the mature marsh was nearly 2-fold lower than in the 7-year-old marsh, and there was no evidence that this was due to light limitation. However, Chl a in fertilized plots was 30% higher than control plots at the youngest site. Daily N fixation decreased with increasing marsh age in summer, when rates were highest at all sites. Autotrophic N fixation (difference between rates in the light and dark) was most important in the summer, but we saw no indication of a shift in dominance between autotrophic and heterotrophic N fixers during marsh development. Estimated annual N fixation was 2- to 3-fold higher in the young marsh (18.3+/-1.5 g N m(-2) year(-1)), than in the intermediate-aged (9.0+/-0.7) or mature marsh (6.1+/-0.5). In the young marshes, N fixation was sufficient to provide a substantial proportion of aboveground S. alterniflora N demand. Our results suggest that both benthic microalgae and S. alterniflora in young salt marshes are N limited, and that this limitation decreases as the marsh matures. The high rates of N fixation by autotrophic and heterotrophic bacteria in the sediment could provide an important source of N for primary producers during marsh development.