Restored Eelgrass (<Emphasis Type="Italic">Zostera marina</Emphasis> L.) as a Refuge for Epifaunal Biodiversity in Mid-Western Atlantic Coastal Bays

As nearshore ecosystems are increasingly degraded by human activities, active restoration is a critical strategy in ensuring the continued provision of goods and services by coastal habitats. After being absent for nearly six decades, over 1800 ha of the foundational species eelgrass (Zostera marina L.) has been successfully re-established in the coastal bays of the mid-western Atlantic, USA, but nothing is known about the recovery of associated animal communities in this region. Here, we determine the patterns and drivers of functional recovery in epifaunal invertebrates associated with the restored eelgrass habitat from 2001 to 2013. After less than a decade, the invertebrate community in the restored bed was richer, more even, and exhibited greater variation in functional traits than a nearby reference bed. Analysis of a suite of environmental and physical variables using random forests revealed these differences were primarily due to the increasing area and density of eelgrass, a direct consequence of ongoing restoration efforts. Based on analysis of functional traits, we propose that the rapid life histories of constituent organisms may have played a key role in their successful recovery. We also speculate that diverse epifaunal communities may have contributed to the restoration success through a well-described mutualism with eelgrass. Given that restored eelgrass now make up 32 % of total seagrass cover in the mid-Atlantic coastal bays, this restoration may conserve regional biodiversity by providing new and pristine habitat, particularly given the general decline of existing eelgrass in this region.     

Eelgrass (<Emphasis Type="Italic">Zostera marina</Emphasis> L.) in the Chesapeake Bay Region of Mid-Atlantic Coast of the USA: Challenges in Conservation and Restoration

Decreases in seagrass abundance reported from numerous locations around the world suggest that seagrass are facing a global crisis. Declining water quality has been identified as the leading cause for most losses. Increased public awareness is leading to expanded efforts for conservation and restoration. Here, we report on abundance patterns and environmental issues facing eelgrass (Zostera marina), the dominant seagrass species in the Chesapeake Bay region in the mid-Atlantic coast of the USA, and describe efforts to promote its protection and restoration. Eelgrass beds in Chesapeake Bay and Chincoteague Bay, which had started to recover from earlier diebacks, have shown a downward trend in the last 5–10 years, while eelgrass beds in the Virginia coastal bays have substantially increased in abundance during this same time period. Declining water quality appears to be the primary reason for the decreased abundance, but a recent baywide dieback in 2005 was associated with higher than usual summer water temperatures along with poor water clarity. The success of eelgrass in the Virginia coastal bays has been attributed, in part, to slightly cooler water due to their proximity to the Atlantic Ocean. A number of policies and regulations have been adopted in this region since 1983 aimed at protecting and restoring both habitat and water quality. Eelgrass abundance is now one of the criteria for assessing attainment of water clarity goals in this region. Numerous transplant projects have been aimed at restoring eelgrass but most have not succeeded beyond 1 to 2 years. A notable exception is the large-scale restoration effort in the Virginia coastal bays, where seeds distributed beginning in 2001 has initiated an expanding recovery process. Our research on eelgrass abundance patterns in the Chesapeake Bay region and the processes contributing to these patterns have provided a scientific background for management strategies for the protection and restoration of eelgrass and insights into the causes of success and failure of restoration efforts that may have applications to other seagrass systems.     

Relative Impacts of Natural Stressors on Life History Traits Underlying Resilience of Intertidal Eelgrass (Zostera marina L.)

Seagrasses are a critical marine habitat and are in decline worldwide. Previous studies have demonstrated that factors such as sediment conditions, resource availability, and desiccation can influence life history transitions and morphology in intertidal eelgrass (Zostera marina L.) and therefore potential for recovery after a disturbance. We combined these factors in an exploratory path model linking environmental conditions to eelgrass vegetative (shoot size and density) and reproductive traits (branching, flowering, seedling recruitment). In this construction, significant path coefficients reveal factors influencing recovery potential. To test the path model, we collected abiotic and eelgrass data at 17 sites in the southern Salish Sea (Washington, USA) and assessed model fit with structural equation modeling. Significant path coefficients linked sediment organic content to shoot size and seedling recruitment, tidal amplitude to reduced flowering, and shoot size and density were inversely correlated. We found no significant links between any morphological or life history trait and nutrient availability, possibly reflecting consistently high nutrients across sites. Variable rates of asexual reproduction and a trade-off between shoot size and density may reflect light limitation in eelgrass’ intertidal range, where light is not expected to be strongly limiting. Overall, structural equation modeling identified organic-rich sediments as relatively more important than desiccation and nutrient conditions for resilience potential of intertidal eelgrass populations in this region. Life history and morphological traits provide eelgrass with recovery mechanisms from disturbance where sediments are muddy, which has implications for both conservation and restoration.     

Subtidal Eelgrass Declines in the Great Bay Estuary,New Hampshire and Maine,USA

Long-term monitoring of eelgrass (Zostera marina L.) beds in the central subtidal portion of the Great Bay Estuary showed declines at both transplanted sites and reference beds. Eelgrass beds transplanted as mitigation for habitat loss from port development reached comparable functions (e.g., primary production, canopy structure) to natural reference sites by the late 1990s, within 6 years of transplanting. Data from 2001 to the present show significant declines in eelgrass parameters (biomass, shoot density, canopy height, leaf area) at all sites, suggesting that these declines are the result of an estuary-wide factor.     

Local Regime Shifts Prevent Natural Recovery and Restoration of Lost Eelgrass Beds Along the Swedish West Coast

Along the Swedish northwest coast, over 60% of the eelgrass meadows have been lost since the 1980s. Despite improved water quality, no recovery has occurred, and restoration is presently considered to mitigate historical losses. However, the factors preventing natural recovery of eelgrass are not known, and it is not clear if conditions would allow restoration. Here, we present the results from 5 years of field studies with the aim of identifying the key processes affecting eelgrass growth and survival at historical eelgrass areas. Continuous light measurements and comparison with historic eelgrass distribution indicate that maximum depth distribution has decreased locally with 1.5–2.3 m in areas that have lost large eelgrass beds in the last 10–30 years. Field studies suggest that wind-driven local resuspension of sediments that are no longer stabilized by eelgrass beds is the main cause behind the deteriorated light conditions. Field experiments show that a combination of low light condition and disturbance from drifting algal mats prevents eelgrass recovery in these areas, whereas the sulfide intrusion from the sediment and dislodgement of shoots by waves had little effect on growth and survival. These results suggest that local regime shifts acting on a scale of 40–200 ha have occurred after the loss of eelgrass beds, where increased sediment resuspension and proliferation of drifting algal mats act as feedback mechanisms that prevent both natural recovery and restoration of eelgrass. The feedbacks appear to be interacting and causing an accelerating loss of eelgrass that is presently spreading to neighboring areas.     

Biomass-Cover Relationship for Eelgrass Meadows

Eelgrass meadows play key roles in coastal ecosystems, and the extent of the standing biomass is focal to address ecosystem functioning. Eelgrass cover is commonly assessed in marine monitoring programs while biomass sampling is destructive and expensive. Therefore, we have proposed a functional relationship that translates eelgrass cover into aboveground biomass using site-specific information on Secchi depth or light attenuation. The relationship was estimated by non-linear regression on 791 combined observations of eelgrass cover and biomass from eight different coastal sites in Denmark. Eelgrass biomass initially increased with cover and flattened out as cover exceeded 40–50 % due to increased self-shading. Decreasing light energy with depth reduced the eelgrass biomass potential (assessed at 100 % cover), and this reduction was stronger for coastal sites with lower water transparency. Moreover, the biomass potential varied seasonally from around 110–140 g DW m^?2 in spring months to a peak of 241 g DW m^?2 in August, consistent with other seasonal studies. The model explained 56 % of the variation in log-transformed biomasses, but significant variation between coastal sites still remained, deviating between ?23 and 39 % from the mean relationship. These site-specific deviations could be due to differences in losses related to grazing, drifting algae and epiphytes, better light capture by dense canopies, as well as differences in how well light conditions within eelgrass meadows are represented by actual measurements of Secchi depth and light attenuation. The relationship can be employed to estimate eelgrass biomass of entire coastal ecosystems from observations of eelgrass cover and depth.     

How Population Decline Can Impact Genetic Diversity: a Case Study of Eelgrass (<Emphasis Type="Italic">Zostera marina</Emphasis>) in Morro Bay,California

Seagrass populations are in decline worldwide. Eelgrass (Zostera marina L.), one of California’s native seagrasses, is no exception to this trend. In the last 8 years, the estuary in Morro Bay, California, has lost 95% of its eelgrass. Population bottlenecks like this one often result in severe reductions in genetic diversity; however, this is not always the case. The decline of eelgrass in Morro Bay provides an opportunity to better understand the effects of population decline on population genetics. Furthermore, the failure of recent restoration efforts necessitates a better understanding of the genetic underpinnings of the population. Previous research on eelgrass in California has demonstrated a link between population genetic diversity and eelgrass bed health, ecosystem functioning, and resilience to disturbance and extreme climatic events. The genetic diversity and population structure of Morro Bay eelgrass have not been assessed until this study. We also compare Morro Bay eelgrass to Bodega Bay eelgrass in Northern California. We conducted fragment length analysis of nine microsatellite loci on 133 Morro Bay samples, and 20 Bodega Bay samples. We found no population differentiation between the remaining beds in Morro Bay and no difference among samples growing at different tidal depths. Comparisons with Bodega Bay revealed that Morro Bay eelgrass contains three first-generation migrants from the north, but Morro Bay remains considerably genetically differentiated from Bodega Bay. Despite the precipitous loss of eelgrass in Morro Bay between 2008 and 2017, genetic diversity remains relatively high and comparable to other populations on the west coast.     

Genetic Structure and Diversity of <Emphasis Type="Italic">Zostera marina</Emphasis> (Eelgrass) in the San Juan Archipelago,Washington, USA

Using data from eight autosomal microsatellite loci, we investigated levels of within- and between-site variation in the seagrass Zostera marina L. (eelgrass) from eight locations in the San Juan Archipelago, located in the northwest corner of Washington, USA. Only 117 of the 365 samples collected were unique individuals, and there were large differences in the estimates of clonality among sites. Site-specific genotypic richness ranged from 0.082 to 0.688, and the distribution of ramets and genets varied widely within sites. No multilocus genotypes were shared between sites. We found significant differences in distribution of alleles and variance in allele frequencies among sites, suggesting substantial genetic population substructuring. We detected low levels of genetic diversity in two sites known to have undergone recent declines and a genetic signature of population expansion in a site known to be increasing. Thus, like elsewhere, we find that genetic studies add an important component to monitoring programs in this region.     

Comparative reproductive success of winter flounder in Long Island Sound: A three-year study (biology,biochemistry, and chemistry)

In a 3-yr study, late prespawning winter flounder were collected from various stations in Long Island Sound (three of them heavily urbanized) and spawned in the laboratory. For comparative purposes, flounder from two sites in the Boston Harbor area were similarly treated in 1987 and 1988. Of the stations in Long Island Sound, New Haven Harbor alone consistently produced low percent viable hatch and small larvae. Boston Harbor produced the smallest larvae of all sites. There were no significant station-to-station differences in lipid utilization during larval development; yolk reserves at stations showing a low percent viable hatch, small larvae, and low embryonic development rate were probably used in part for stress metabolism. No significant differences in concentrations of polychlorinated biphenyls for collections from Long Island Sound were found either in livers of spawned fish, in sediments, or in eggs of winter flounder. The very low metal concentrations in winter flounder eggs showed no relation to the degree of metal contamination found at stations in Long Island Sound and Boston Harbor.     

Restoring Resiliency: Case Studies from Pacific Northwest Estuarine Eelgrass (<Emphasis Type="Italic">Zostera marina</Emphasis> L.) Ecosystems

An objective of many ecological restoration projects is to establish resilience to disturbances. Eelgrass (Zostera marina L.) represents a useful model to evaluate resilience because the plant community is dominated by one species and the estuarine environment is dynamic. Our studies of planted and reference plots used shoot density monitoring data from three projects spanning 3 to 12 years. Data show that eelgrass can recover from major shifts in pond position and shape on sandflats, as well as natural disturbances causing >20-fold change in density. However, cumulative effects of multiple stressors on unestablished plantings suggest algal blooms of unusual magnitude can tip normally marginal conditions to unfavorable. Thus, potential resilience appears to depend on landscape conditions. A dynamic equilibrium was evinced in even the deepest, lowest-density plantings, probably associated with light-mediated carrying capacity and vegetative belowground production characteristic of the Pacific Northwest. We recommend eight resilience-related planning elements to reduce uncertainties in eelgrass restoration.     

Light Requirements for Growth and Survival of Eelgrass (<Emphasis Type="Italic">Zostera marina</Emphasis> L.) in Pacific Northwest (USA) Estuaries

We developed light requirements for eelgrass in the Pacific Northwest, USA, to evaluate the effects of short- and long-term reductions in irradiance reaching eelgrass, especially related to turbidity and overwater structures. Photosynthesis-irradiance experiments and depth distribution field studies indicated that eelgrass productivity was maximum at a photosynthetic photon flux density (PPFD) of about 350–550 μmol quanta m⁻² s⁻¹. Winter plants had approximately threefold greater net apparent primary productivity rate at the same irradiance as summer plants. Growth studies using artificial shading as well as field monitoring of light and eelgrass growth indicated that long-term survival required at least 3 mol quanta m⁻² day⁻¹ on average during spring and summer (i.e., May-September), and that growth was saturated above about 7 mol quanta m⁻² day⁻¹. We conclude that non-light-limited growth of eelgrass in the Pacific Northwest requires an average of at least 7 mol quanta m⁻² day⁻¹ during spring and summer and that long-term survival requires a minimum average of 3 mol quanta m⁻² day⁻¹.     

Twelve-Year Mapping and Change Analysis of Eelgrass (<Emphasis Type="Italic">Zostera marina</Emphasis>) Areal Abundance in Massachusetts (USA) Identifies Statewide Declines

In 1994, 1995, and 1996, seagrasses in 46 of the 89 coastal embayments and portions of seven open-water near-shore areas in Massachusetts were mapped with a combination of aerial photography, digital imagery, and ground truth verification. In the open-water areas, 9,477.31 ha of seagrass were identified, slightly more than twice the 4,846.2 ha detected in the 46 coastal embayments. A subset of the 46 embayments, including all regions of the state were remapped in 2000, 2001, and 2002 and again in 2006 and 2007. We detected a wide range of changes from increases as high as 29% y⁻¹ in Boston Harbor to declines as large as −33% y⁻¹ in Salem Harbor. One embayment, Waquoit Bay, lost all of its seagrass during the mapping period. For the 12-year change analysis representing all geographic regions of the state, only three embayments exhibited increases in seagrass coverage while 30 of the original 46 embayments showed some indication of decline. For the decadal period, rates of decline in the individual embayments ranged from −0.06% y⁻¹ to as high as −14.81% y⁻¹. The median rate of decline by region ranged from −2.21% y⁻¹ to −3.51% y⁻¹ and was slightly less than the recently reported global rate of decline for seagrasses (−3.7% y⁻¹). Accounting for the gains in three of the embayments, 755.16 ha (20.6%) of seagrass area originally detected was lost during the mapping interval. The results affirm that previously reported losses in a few embayments were symptomatic of more widespread seagrass declines in Massachusetts. State and Federal programs designed to improve environmental quality for conservation and restoration of seagrasses in Massachusetts should continue to be a priority for coastal managers.     

Vitellogenin in winter flounder (Pleuronectes americanus) from Long Island Sound and Boston Harbor

Vitellogenin is an egg-yolk precursor protein in teleosts which is crucial to the survival of larvae. Manufactured in the liver, where pollutants are known to accumulate, and transported to the ovary by the blood, its synthesis by the liver or uptake by the gonad can be compromised by accumulation of xenobiotics. In three studies, winter flounder (Pleuronectes americanus) blood samples were taken to determine normal levels of vitellogenin during the reproductive cycle, and to learn how its production might be affected in degraded environments. Specifically, these studies followed the seasonal cycle of vitellogenin production in winter flounder through monthly sampling at relatively clean (Shoreham, New York) and degraded areas (Black Rock and New Haven harbors, Connecticut) in Long Island Sound; examined the relationship between parental vitellogenin levels and survival of offspring by sampling fish that had been spawned at the Milford Laboratory for a reproductive success study; and determined the effect of gross liver lesions on vitellogenin production by sampling flounder from Boston Harbor, Massachusetts, which have been reported to have a high prevalence of liver tumors. Blood vitellogenin levels were determined by measuring alkali-labile phosphate (ALP). Large fish (>30 cm) from the two degraded sites had elevated serum ALP levels relative to those from the clean area. Lowered total ovarian lipid levels in large fish from Black Rock Harbor suggested impaired vitellogenin uptake. There were no significant differences in serum ALP among the small (≤30 cm) fish from the three sampling sites. Boston Harbor flounder with gross liver lesions had lower ALP values than fish without such lesions. There were no significant differences in ALP values among the spawned fish.     

Large-Scale Differences in Community Structure and Ecosystem Services of Eelgrass (<Emphasis Type="Italic">Zostera marina</Emphasis>) Beds Across Three Regions in Eastern Canada

Eelgrass (Zostera marina) forms extensive beds in temperate coastal and estuarine environments worldwide and provides important ecosystem services, including habitat for a wide range of species as well as nutrient cycling and carbon storage. However, little is known about how eelgrass ecosystem structure and services differ naturally among regions. Using large-scale field surveys, we examined differences in eelgrass bed structure, carbon and nitrogen storage, community composition, and habitat services across three distinct regions in Eastern Canada. We focused on eelgrass beds with low anthropogenic impacts to compare natural differences. In addition, we analyzed the relationships of eelgrass bed structure with environmental conditions, and species composition with bed structure and environmental conditions, to elucidate potential drivers of observed differences. Our results indicate that regional differences in eelgrass bed structure were weakly correlated with water column properties, whereas differences in carbon and nitrogen storage were mainly driven by differences in eelgrass biomass. There were distinct regional differences in species composition and diversity, which were particularly linked to temperature, as well as eelgrass bed structure indicating differences in habitat provision. Our results highlight natural regional differences in ecosystem structure and services which could inform spatial management and conservation strategies for eelgrass beds.     

Regulation of eelgrass (Zostera marina) cover along depth gradients in Danish coastal waters

A large data set, collected under the national Danish monitoring program, was used to evaluate the importance of photon flux density (PFD), relative wave exposure (REI), littoral slope, and salinity in regulating eelgrass cover at different depth intervals in Danish coastal waters. Average eelgrass cover exhibited a bell-shaped pattern with depth, reflecting that different factors regulate eelgrass cover at shallow- and deep-water sites. The multiple logistic regression analysis was used to identify regulating factors and determine their role in relation to eelgrass cover at different depth intervals. PFD, REI, and salinity were main factors affecting eelgrass cover while littoral slope had no significant effect. Eelgrass cover increased with increasing PFD at water depths of more than 2 m, while cover was in versely related to REI in shallow water. This pattern favored eelgrass cover at intermediate depths where levels of PFD and REI were moderate. Salinity had a minor, but significant, effect on eelgrass cover that is most likely related to the varying costs of osmoregulation with changing salinity. The analysis provided a useful conceptual framework for understanding the factors that regulate eelgrass abundance with depth. Although the regression model was statistically significant and included the factors generally considered most important in regulating eelgrass cover, its explanatory power was low, especially in shallow water. The largest discrepancies between predicted and observed values of cover appeared in cases where no eelgrass occurred despite sufficient light and moderate levels of exposure (almost 50% of all observations). These discrepancies suggest that population losses due to stochastic phenomena, such as extreme wind events, played an important regulating role that is not adequately described by average exposure levels. A more thorough knowledge of the importance of such loss processes and the time scales involved in recovery of seagrass populations after a severe disturbance are necessary if we are to understand the regulation of seagrass distribution in shallow coastal areas more fully.     

Long-term Trends of Benthic Habitats Related to Reduction in Wastewater Discharge to Boston Harbor

A combination of methods (infaunal grabs and sediment profile cameras) were used to monitor the response of Boston Harbor benthic habitats to reductions in wastewater associated with movement of the outfalls to the mouth of the harbor and then offshore. From 1992 to 2006, there was strong evidence that benthic habitats within Boston Harbor have shifted from a more anaerobic state to a more aerobic state and that these changes are directly related to changes in carbon loading associated with outfall placement and improvements in wastewater treatment. Over the period of 1992 to 2000, when the ocean outfall started to operate, there was >90% reduction in organic loadings to Boston Harbor from 11,400 to 1,200 t C per year. There were also corresponding decreases in primary production due to reduced nutrient loadings. The most apparent change in harbor benthos was the widespread increase in 1992 and subsequent decline by 2005 in Ampelisca spp. tube mats. The long-term increase in thickness of the apparent color redox potential discontinuity layer was consistent with reductions in organic loading and increases in bioturbation. The optimal organic loading for maintaining large areas of amphipod tube mats and high bioturbation rates was around 500 g C per square meter per year. Above and below this level, the area of tube mats in Boston Harbor declined.     

Variability in habitat use by young-of-the-year winter flounder,<Emphasis Type="Italic">Pseudopleuronectes americanus</Emphasis>, in three northeastern U.S. estuaries

We compared distribution and abundance by habitat for age-0, young-of-the-year (YOY) winter flounder,Pseudopleuronectes americanus, in three estuaries (Hammonasset River, Navesink River, and Great Bay-Little Egg Harbor) in the northeastern United States to better define essential fish habitat (EFH). Two replicates of five representative habitats were sampled in most estuaries: eelgrass (Zostera marina), unvegetated areas adjacent to eelgrass, macroalgae, (primarilyUlva lactuca), unvegetated areas adjacent to macroalgae, and tidal marsh creeks. Fish were sampled every two weeks, May through October 1995 and 1996, with a beam-trawl (1-m width, 3-mm mesh net). Abundance of YOY winter flounder was highest in the Navesink River estuary and similar between years, but was significantly lower and differed between years in the Great Bay-Little Egg Harbor and Hammonasset River estuaries. Annual temperature differences appear to influence estuary use by YOY. In the years and estuaries studied, where habitat-related differences in abundance were significant, YOY were found in higher densities in unvegetated areas adjacent to eelgrass. The exception was in the Hammonasset River in 1995 when densities were higher in eelgrass. We conclude that the type of habitat most important to YOY winter flounder varies among estuaries and as a result, care should be taken in defining EFH, based only on limited spatial and temporal sampling.     

Post-settlement alteration of spatial patterns of soft shell clam (<Emphasis Type="Italic">Mya arenaria</Emphasis>) recruits

To examine the roles of settlement and early post-settlement processes in patterns of recruitment of the soft shell clamMya arenaria, abundance of juvenileMya at three intertidal sites in Barnstable Harbor, Massachusetts, was monitored over two settlement seasons. Two peaks of settlement occurred in 1998 (July and September) and one peak was recorded in June 1999, indicating that a late season settlement event is not a consistent feature at this site. Abundance of recent settlers (i.e., early recruits, < 1 week past settlement) varied significantly among the tidal flats (sites) that were separated by hundreds of meters to kilometers, but not among plots meters apart. Differences in abundance of settlers likely resulted in these differences in early-recruit abundance among sites. Settlement was greatest at the site with the greatest variability in flow speed. Sites also differed to some extent in their sediment characteristics and macrofaunal assemblages, which may influence larval substrate choice. Between-site differences in abundance ofMya decreased after settlement. The rate of decline of abundance varied among cohorts and sites. Comparison of abundance of recent settlers (up to 145,000 m⁻²) to that of juveniles > 3-mm shell length at the end of the settlement season (up to 60 m⁻²) indicated large losses of individuals during the early post-settlement period. This study demonstrates that spatial patterns inMya abundance can change substantially during the early post-settlement period, and that high mortality rates can result in cohorts contributing little to the population size even when rates of settlement are high.