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.

Seagrasses are important foundation species in shallow coastal ecosystems that provide critical ecosystem services including stabilizing sediment, sequestering carbon and nutrients, and providing habitat and an energy source for a diverse fauna. We followed the recovery of functional (primary productivity, carbon and nitrogen sequestration, sediment deposition) and structural (shoot density, biomass, plant morphometrics) attributes of Zostera marina (eelgrass) meadows in replicate large plots (0.2 to 0.4 ha) restored by seeding in successive years, resulting in a chrono sequence of sites from 0 (unvegetated) to 9 yr since seeding. Shoot density was the structural metric that changed most significantly, with an initial 4 yr lag, and a rapid, linear increase in plots 6 to 9 yr after seeding. Changes in Z. marina aerial productivity, sediment organic content, and exchangeable ammonium showed a similar trend with an initial 4 yr lag period before differences were observed from initial bare sediment conditions. After 9 yr, Z. marina meadows had 20× higher rates of areal productivity than 1 to 3 yr old meadows, double the organic matter and exchangeable ammonium concentrations, 3× more carbon and 4× more nitrogen, and had accumulated and retained finer particles than bare, unvegetated sediments. These results demonstrate the reinstatement of key ecosystem services with successful large-scale restoration, although none of the parameters reached an asymptote after 9 yr, indicating that at least a decade is required for these attributes to be fully restored, even in an area with high habitat suitability. Survivorship along a depth gradient showed that ~1.6 m (mean sea level) is the maximum depth limit for Z. marina, which matches the 'tipping point' for survival predicted for this system from a non-linear hydro dynamic/seagrass growth model.

Genetic diversity is positively associated with plant fitness, stability, and the provision of ecosystem services. Preserving genetic diversity is therefore considered an important component of ecosystem restoration as well as a measure of its success. We examined the genetic diversity of restored Zostera marina meadows in a coastal bay system along the USA mid-Atlantic coast using microsatellite markers to compare donor and recipient meadows. We show that donor meadows in Chesapeake Bay have high genetic diversity and that this diversity is maintained in meadows restored with seeds in the Virginia coastal bays. No evidence of inbreeding depression was detected (F IS −0.2 to 0) in either donor or recipient meadows, which is surprising because high levels of inbreeding were expected following the population contractions that occurred in Chesapeake Bay populations due to disease and heat stress. Additionally, there was no evidence for selection of genotypes at the restoration sites, suggesting that as long as donor sites are chosen carefully, issues that diminish fitness and survival such as heterosis or out-breeding depression can be avoided. A cluster analysis showed that, in addition to the Chesapeake Bay populations that acted as donors, the Virginia coastal bay populations shared a genetic signal with Chincoteague Bay populations, their closest neighbor to the north, suggesting that natural recruitment into the area may be occurring and augmenting restored populations. We hypothesize that the high genetic diversity in seagrasses restored using seeds rather than adult plants confers a greater level of ecosystem resilience to the restored meadows.KEY WORDS: Seagrass · Zostera marina · Restoration · Genetic diversity · Microsatellite DNA Resale or republication not permitted without written consent of the publisher Contribution to the Theme Section 'Eelgrass recovery'OPEN PEN ACCESS CCESS

Summary1. Ecological restoration assists the recovery of degraded ecosystems; however, restoration can have deleterious effects such as outbreeding depression when source material is not chosen carefully and has non-local adaptations. 2. We surveyed 23 eelgrass (Zostera marina L.) populations along the North American Atlantic coast to evaluate genetic structure and connectivity among restored and naturally recruited populations. 3. While populations along the North America Atlantic coast were genetically distinctive, significant migration was detected among populations. All estimates of connectivity (F ST , migration rate base on rare alleles, and Bayesian modelling) showed a general north to south pattern of migration, corresponding to the typical long-shore currents in this region. 4. Individual naturally recruited meadows in the Virginia coastal bays appear to be the result of dispersal from different meadows north of the region. This supports the hypothesis that recruitment into this region is typically a slow, episodic process rather than a permanent, continuous connection between the populations. 5. While natural recovery of populations that were catastrophically lost in the 1930s has been slow, large-scale seed-based restoration has been very successful at quickly restoring landscape-scale areal coverage (over 1600 ha in just 10 years). Our results show that restoration was also successful at restoring meadows with high genetic diversity. Naturally recruited meadows were less diverse and exhibited signs of genetic drift. 6. Synthesis. Our analyses demonstrate that metapopulation dynamics are important to the natural recovery of seagrass ecosystems that have experienced catastrophic loss over large spatial scales; however, natural recovery processes are slow and inefficient at recovering genetic diversity and population structure when recruitment barriers exist, such as a limited seed source. Seed-based restoration provides a greater abundance of propagules, rapidly facilitates the recovery of populations with higher genetic diversity, and when seed sources are chosen carefully protects regional genetic structure. Firstorder estimates indicated that the genetic diversity achieved by active restoration in 10 years would have otherwise taken between 125 and 185 years to achieve through natural recruitment events.

Ecosystem restoration is often costly, but can be effective at increasing biodiversity and ecosystem services. We used a case study-reseeding seagrass to a coastal lagoon-to demonstrate the value of enhanced ecosystem services as a result of restoration. We modeled the recovery of areal plant coverage in a system where seagrasses were lost due to disease and disturbance, and estimated the value of the returned functions of nitrogen removal and carbon sequestration. We estimated, as of 2010, that this restoration removes 170 ton of nitrogen per year via denitrificiation and sequesters carbon at a rate of 630 tons carbon per year in the sediment. Further, we estimated that natural recovery would take more than 100 years to reach the areal coverage achieved by restoration using seeds in just 10 years. Restoration enhanced this recovery, and the earlier establishment of plants results in a net gain of at least 4,100 ton of nitrogen removed from the system via denitrification and 15,000 ton of carbon sequestered in the sediment. These services have significant ecological and societal value.

Growing evidence shows that increasing global temperature causes population declines and latitudinal shifts in geographical distribution for plants living near their thermal limits. Yet, even populations living well within established thermal limits of a species may suffer as the frequency and intensity of warming events increase with climate change. Adaptive response to this stress at the population level depends on the presence of genetic variation in thermal tolerance in the populations in question, yet few data exist to evaluate this. In this study, we examined the immediate effects of a moderate warming event of 4.5°C lasting 5 weeks and the legacy effects after a 5 week recovery on different genotypes of the marine plant Zostera marina (eelgrass). We conducted the experiment in Bodega Bay, CA USA, where average summer water temperatures are 14–15°C, but extended warming periods of 17–18°C occur episodically. Experimental warming increased shoot production by 14% compared to controls held at ambient temperature. However, after returning temperature to ambient levels, we found strongly negative, delayed effects of warming on production: shoot production declined by 27% and total biomass decreased by 50% relative to individuals that had not been warmed. While all genotypes’ production decreased in the recovery phase, genotypes that grew the most rapidly under benign thermal conditions (control) were the most susceptible to the detrimental effects of warming. This suggests a potential tradeoff in relative performance at normal vs. elevated temperatures. Modest short-term increases in water temperature have potentially prolonged negative effects within the species’ thermal envelope, but genetic variation within these populations may allow for population persistence and adaptation. Further, intraspecific variation in phenology can result in maintenance of population diversity and lead to enhanced production in diverse stands given sufficient frequency of warming or other stress events.

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