Population genetic patterns across the native and invasive range of a widely distributed seagrass: Phylogeographic structure, invasive history and conservation implications.

Aim: The seagrass Zostera japonica is a dramatically declined endemic species in the Northwestern Pacific from the (sub)tropical to temperate areas, however, it is also an introduced species along the Pacific coast of North America from British Columbia to northern California. Understanding the population's genetic patterns can inform the conservation and management of this species. Location: North Pacific. Methods: We used sequences of the nuclear rDNA internal transcribed spacer (ITS) and chloroplast trnK intron maturase (matK), and 24 microsatellite loci to survey 34 native and nonnative populations (>1000 individuals) of Z. japonica throughout the entire biogeographic range. We analysed the phylogeographic relationship, population genetic structure and genetic diversity of all populations and inferred possible origins and invasion pathways of the nonnative ones. Results: All markers revealed a surprising and significant deep divergence between northern and southern populations of Z. japonica in the native region separated by a well-established biogeographical boundary. A secondary contact zone was found along the coasts of South Korea and Japan. Nonnative populations were found to originate from the central Pacific coast of Japan with multiple introductions from at least two different source populations, and secondary spread was likely aided by waterfowl. Main Conclusions: The divergence of the two distinct clades was likely due to the combined effects of historical isolation, adaptation to distinct environments and a contemporary physical barrier created by the Yangtze River, and the warm northward Kuroshio Current led to secondary contact after glacial separation. Existing exchanges among the nonnative populations indicate the potential for persistence and further expansion. This study not only helps to understand the underlying evolutionary potential of a widespread seagrass species following global climate change but also provides valuable insights for conservation and restoration.

A Pleistocene legacy structures variation in modern seagrass ecosystems.

Distribution of Earth's biomes is structured by the match between climate and plant traits, which in turn shape associated communities and ecosystem processes and services. However, that climate-trait match can be disrupted by historical events, with lasting ecosystem impacts. As Earth's environment changes faster than at any time in human history, critical questions are whether and how organismal traits and ecosystems can adjust to altered conditions. We quantified the relative importance of current environmental forcing versus evolutionary history in shaping the growth form (stature and biomass) and associated community of eelgrass (Zostera marina), a widespread foundation plant of marine ecosystems along Northern Hemisphere coastlines, which experienced major shifts in distribution and genetic composition during the Pleistocene. We found that eelgrass stature and biomass retain a legacy of the Pleistocene colonization of the Atlantic from the ancestral Pacific range and of more recent within-basin bottlenecks and genetic differentiation. This evolutionary legacy in turn influences the biomass of associated algae and invertebrates that fuel coastal food webs, with effects comparable to or stronger than effects of current environmental forcing. Such historical lags in phenotypic acclimatization may constrain ecosystem adjustments to rapid anthropogenic climate change, thus altering predictions about the future functioning of ecosystems.

The biogeography of community assembly: latitude and predation drive variation in community trait distribution in a guild of epifaunal crustaceans.

While considerable evidence exists of biogeographic patterns in the intensity of species interactions, the influence of these patterns on variation in community structure is less clear. Studying how the distributions of traits in communities vary along global gradients can inform how variation in interactions and other factors contribute to the process of community assembly. Using a model selection approach on measures of trait dispersion in crustaceans associated with eelgrass (Zostera marina) spanning 30° of latitude in two oceans, we found that dispersion strongly increased with increasing predation and decreasing latitude. Ocean and epiphyte load appeared as secondary predictors; Pacific communities were more overdispersed while Atlantic communities were more clustered, and increasing epiphytes were associated with increased clustering. By examining how species interactions and environmental filters influence community structure across biogeographic regions, we demonstrate how both latitudinal variation in species interactions and historical contingency shape these responses. Community trait distributions have implications for ecosystem stability and functioning, and integrating large-scale observations of environmental filters, species interactions and traits can help us predict how communities may respond to environmental change.

Variability in blue carbon storage related to biogeochemical factors in seagrass meadows off the coast of the Korean peninsula.

Coastal vegetated habitats such as mangroves, salt marshes, and seagrasses, referred to as blue carbon ecosystems, play an important role in climate change mitigation by an effective CO2 capture from atmosphere and water columns and long-term organic carbon (Corg) storage in sediments. Although seagrass meadows are considered intense carbon sinks, information on regional variability in seagrass blue carbon stock and factors influencing its capacity still remain sparse. In the present study, seagrass blue carbon storage by measuring Corg stocks in sediments and living seagrass biomass, and carbon accumulation rates (CARs) in seagrass meadows were estimated along the Korean coast. Factors affecting variability in Corg stocks were also analyzed using partial least squares (PLS) regression and principal component analysis (PCA). Projected Corg stocks in sediment, extrapolated to a depth 1 m, exhibited substantial variability among sites, ranging from 49.91 to 125.71 Mg C ha-1. The majority of Corg (96-99%) was stored in sediments, whereas the contribution of living biomass was minor. PLS regression and PCA indicated that Corg stocks in seagrass meadows are strongly associated with sediment characteristics such as dry bulk density and water and mud content. Among seagrass traits, above- to below-ground biomass ratio was significantly related to the quantity of Corg stocks in seagrass meadows. Because of the high spatial variability in Corg stocks and CARs, local and regional differences in seagrass blue carbon storage should be considered to accurately assess the climate change mitigation potential of seagrass ecosystems.

Coastal Sediment Nutrient Enrichment Alters Seagrass Blue Carbon Sink Capacity.

The seagrass ecosystem is among the most efficient natural carbon sinks that can contribute to climate change mitigation. However, little is known about the effects of coastal nutrient enrichment caused by anthropogenic activities and/or climate change on the capacity of the seagrass blue carbon sink. Our experimental manipulations of sediment nutrient enrichment shifted the blue carbon sink capabilities of seagrass meadows. Sediment nutrient enrichment significantly increased the nutrient content of seagrass litter, stimulating the decomposition of rhizome + root litter by ∼10% while retarding the decomposition of leaf litter by ∼5%. Sediment N + P enrichment increased seagrass growth and litter production, while enrichment of N or P alone did not. Organic carbon (Corg) stocks in the surface sediments (0-5 cm) were 34% higher than those in the control with N + P enrichment due to high litter production and the low decomposition rate of nutrient-enriched leaf litter. However, Corg stocks in the subsurface sediments (5-20 cm) did not increase with sediment nutrient enrichment, which is likely due to accelerated decomposition of rhizome + root litter. Our findings suggest that nutrient loading in coastal sediments alters the blue carbon sink and storage capacities in seagrass meadows by changing the rates of carbon sequestration and decomposition.

Joint effects of patch edges and habitat degradation on faunal predation risk in a widespread marine foundation species.

Human activities degrade and fragment coastal marine habitats, reducing their structural complexity and making habitat edges a prevalent seascape feature. Though habitat edges frequently are implicated in reduced faunal survival and biodiversity, results of experiments on edge effects have been inconsistent, calling for a mechanistic approach to the study of edges that explicitly includes indirect and interactive effects of habitat alteration at multiple scales across biogeographic gradients. We used an experimental network spanning 17 eelgrass (Zostera marina) sites across the Atlantic and Pacific oceans and the Mediterranean Sea to determine (1) if eelgrass edges consistently increase faunal predation risk, (2) whether edge effects on predation risk are altered by habitat degradation (shoot thinning), and (3) whether variation in the strength of edge effects among sites can be explained by biogeographical variability in covarying eelgrass habitat features. Contrary to expectations, at most sites, predation risk for tethered crustaceans (crabs or shrimps) was lower along patch edges than in patch interiors, regardless of the extent of habitat degradation. However, the extent to which edges reduced predation risk, compared to the patch interior, was correlated with the extent to which edges supported higher eelgrass structural complexity and prey biomass compared to patch interiors. This suggests an indirect component to edge effects in which the impact of edge proximity on predation risk is mediated by the effect of edges on other key biotic factors. Our results suggest that studies on edge effects should consider structural characteristics of patch edges, which may vary geographically, and multiple ways that humans degrade habitats.

Climate drives the geography of marine consumption by changing predator communities.

The global distribution of primary production and consumption by humans (fisheries) is well-documented, but we have no map linking the central ecological process of consumption within food webs to temperature and other ecological drivers. Using standardized assays that span 105° of latitude on four continents, we show that rates of bait consumption by generalist predators in shallow marine ecosystems are tightly linked to both temperature and the composition of consumer assemblages. Unexpectedly, rates of consumption peaked at midlatitudes (25 to 35°) in both Northern and Southern Hemispheres across both seagrass and unvegetated sediment habitats. This pattern contrasts with terrestrial systems, where biotic interactions reportedly weaken away from the equator, but it parallels an emerging pattern of a subtropical peak in marine biodiversity. The higher consumption at midlatitudes was closely related to the type of consumers present, which explained rates of consumption better than consumer density, biomass, species diversity, or habitat. Indeed, the apparent effect of temperature on consumption was mostly driven by temperature-associated turnover in consumer community composition. Our findings reinforce the key influence of climate warming on altered species composition and highlight its implications for the functioning of Earth's ecosystems.

Factors controlling the vertical zonation of the intertidal seagrass, Zostera japonica in its native range in the northwestern Pacific.

The desiccation tolerance of the intertidal seagrass Zostera japonica has been demonstrated in a number of studies; however, the factors limiting expansion of intertidal seagrass species into subtidal zones remain controversial. We transplanted Z. japonica shoots from the intermediate intertidal zone into the plots with and without Z. marina shoots in both the lower intertidal and shallow subtidal zones to investigate the factors controlling Z. japonica growth in these zones. Daily photon flux density at the Z. japonica canopy level was attenuated by both water depth and coexisting Z. marina shoots but more strongly by Z. marina shoots than water depth in the transplant plots. The shoot density and biomass of Z. japonica transplants were significantly lower in transplant plots in the subtidal zone than in the lower intertidal zone. Although the photon flux density was significantly lower in transplant plots containing Z. marina shoots, the growth of Z. japonica transplants did not differ significantly between plots with and those without Z. marina shoots. Z. japonica transplants exhibited photoacclimatory responses such as increased shoot height and chlorophyll content under the lower-light conditions, offsetting the reduced light availability so that no significant differences in transplant growth occurred between plots with and those without Z. marina shoots. As the growth of Z. japonica transplants decreased significantly in the subtidal zone, the interactive effects of environmental stresses associated with tidal inundation and reduced light availability may restrict penetration of the intertidal seagrass Z. japonica into the subtidal zone. The persistence of high photosynthetic performance after air exposure and a regular arrangement of the densely overlapped leaves atop wet sediments may be desiccation tolerance mechanisms for Z. japonica in the intertidal zone.

Heavy metal accumulation and phytoremediation potential by transplants of the seagrass Zostera marina in the polluted bay systems.

Although seagrasses can incorporate heavy metals from the marine environment, few studies have been conducted on heavy metal uptake and phytoremediation potential by seagrass transplants in the heavy metal contaminated sediments. Zostera marina shoots were transplanted in two polluted bay systems on Korean coasts to evaluate the heavy metal contaminations in sediments and the possibility of using Z. marina transplants as a bioindicator and phytoremediation agent. The major concentrated metals in sediments were As, Cu, Fe, and Pb in Jaran Bay, and Cd, Co, Zn, and Hg in Onsan Bay. The Co, Zn, Pb, and Hg concentrations in Z. marina tissues reflected the sediment heavy metal concentrations, and thus the tissue heavy metal concentrations may be used as bio-indicators of the metal contaminations. Since Z. marina transplants accumulated a great amount of heavy metals in their tissues, they may have the phytoremediation potential for the heavy metal contaminated sediments.

Latitude, temperature, and habitat complexity predict predation pressure in eelgrass beds across the Northern Hemisphere.

Latitudinal gradients in species interactions are widely cited as potential causes or consequences of global patterns of biodiversity. However, mechanistic studies documenting changes in interactions across broad geographic ranges are limited. We surveyed predation intensity on common prey (live amphipods and gastropods) in communities of eelgrass (Zostera marina) at 48 sites across its Northern Hemisphere range, encompassing over 37° of latitude and four continental coastlines. Predation on amphipods declined with latitude on all coasts but declined more strongly along western ocean margins where temperature gradients are steeper. Whereas in situ water temperature at the time of the experiments was uncorrelated with predation, mean annual temperature strongly positively predicted predation, suggesting a more complex mechanism than simply increased metabolic activity at the time of predation. This large-scale biogeographic pattern was modified by local habitat characteristics; predation declined with higher shoot density both among and within sites. Predation rates on gastropods, by contrast, were uniformly low and varied little among sites. The high replication and geographic extent of our study not only provides additional evidence to support biogeographic variation in predation intensity, but also insight into the mechanisms that relate temperature and biogeographic gradients in species interactions.

Genetic identification and evolutionary trends of the seagrass Halophila nipponica in temperate coastal waters of Korea.

Although seagrass species in the genus Halophila are generally distributed in tropical or subtropical regions, H. nipponica has been reported to occur in temperate coastal waters of the northwestern Pacific. Because H. nipponica occurs only in the warm temperate areas influenced by the Kuroshio Current and shows a tropical seasonal growth pattern, such as severely restricted growth in low water temperatures, it was hypothesized that this temperate Halophila species diverged from tropical species in the relatively recent evolutionary past. We used a phylogenetic analysis of internal transcribed spacer (ITS) regions to examine the genetic variability and evolutionary trend of H. nipponica. ITS sequences of H. nipponica from various locations in Korea and Japan were identical or showed very low sequence divergence (less than 3-base pair, bp, difference), confirming that H. nipponica from Japan and Korea are the same species. Halophila species in the section Halophila, which have simple phyllotaxy (a pair of petiolate leaves at the rhizome node), were separated into five well-supported clades by maximum parsimony analysis. H. nipponica grouped with H. okinawensis and H. gaudichaudii from the subtropical regions in the same clade, the latter two species having quite low ITS sequence divergence from H. nipponica (7-15-bp). H. nipponica in Clade I diverged 2.95 ± 1.08 million years ago from species in Clade II, which includes H. ovalis. According to geographical distribution and genetic similarity, H. nipponica appears to have diverged from a tropical species like H. ovalis and adapted to warm temperate environments. The results of divergence time estimates suggest that the temperate H. nipponica is an older species than the subtropical H. okinawensis and H. gaudichaudii and they may have different evolutionary histories.

Photoacclimatory Responses of Zostera marina in the Intertidal and Subtidal Zones.

Photoacclimatory responses of the seagrass Zostera marina in the intertidal and subtidal zones were investigated by measuring chlorophyll a fluorescence parameters, photosynthetic pigments, leaf δ13C values, and shoot morphology in two bay systems. Intertidal plants had higher carotenoid concentrations than subtidal plants to avoid photodamage under excess light conditions during the day. The maximum relative electron transport rate (rETRmax) and minimum saturation irradiance (Ek) of the intertidal plants were higher than those of the subtidal plants, whereas photosynthetic efficiency (α) and maximum quantum yield (Fv/Fm) were higher in subtidal plants. The intertidal plants also had significantly greater Stern-Volmer non-photochemical quenching (NPQ) than that of the subtidal plants. These results suggest that the subtidal plants photoacclimated to use limited light more efficiently, and the intertidal plants exhibited photosynthetic responses to minimize photodamage at excess irradiance. The δ13C values of leaf tissues were more negative in the intertidal plants than those in the subtidal plants, suggesting that the intertidal plants used atmospheric or dissolved CO2 for photosynthesis during emersion. Effective quantum yield (ΔF/Fm´) in the intertidal plants decreased more slowly after emersion than that in the subtidal plants, indicating higher desiccation tolerance of the intertidal plants. The intertidal plants also recovered more rapidly from desiccation damage than the subtidal plants, suggesting photosynthetic adaptation to desiccation stress. The photosynthetic plasticity of Z. marina in response to variable environmental conditions most likely allows this species to occur in the intertidal and subtidal zones.

An evaluation of leaf biomass : length ratio as a tool for nondestructive assessment in eelgrass (Zostera marina L.).

The characterization of biomass and its dynamics provides valuable information for the assessment of natural and transplanted eelgrass populations. The need for simple, nondestructive assessments has led to the use of the leaf biomass-to-length ratio for converting leaf-length measurements, which can be easily obtained, to leaf growth rates through the plastochrone method. Using data on leaf biomass and length collected in three natural eelgrass populations and a mesocosm, we evaluated the suitability of a leaf weight-to-length ratio for nondestructive assessments. For the data sets considered, the isometric scaling that sustains the weight-to-length proxy always produced inconsistent fittings, and for leaf-lengths greater than a threshold value, the conversion of leaf length to biomass generated biased estimations. In contrast, an allometric scaling of leaf biomass and length was highly consistent in all the cases considered. And these nondestructive assessments generated reliable levels of reproducibility in leaf biomass for all the ranges of variability in leaf lengths. We argue that the use of allometric scaling for the representation of leaf biomass in terms of length provides a more reliable approach for estimating eelgrass biomass.

An effective transplanting technique using shells for restoration of Zostera marina habitats.

Significant declines in seagrass coverage have occurred in many parts of the world. In recent decades, transplanting projects for seagrass restoration at die-off areas have been attempted, but most current seagrass transplanting techniques are cost and labor intensive. We have developed a new seagrass transplanting method in which oyster shells are used as an anchoring device, and does not require SCUBA diving for sub-tidal planting. Here, we tested the shell method for feasibility and efficiency in large-scale seagrass restoration. Planting units consisting of two Zostera marina shoots anchored to one oyster shell were dropped from a boat to settle on the sediment at the test site. Four transplanting trials were conducted throughout the experimental period (December 2003, January, February, and November 2004) in Koje Bay on the southern coast of Korea. Eelgrass shoots planted using the shell method successfully established at the test areas, and the survival rates of transplants were comparable to those obtained using other common planting techniques. The transplant shoot density declined during the first 2-3 months following transplantation due to the initial transplant shock, and then surviving shoots became established at the sites and produced new lateral shoots after these periods. Plant size and leaf productivity of transplants 7 months post-transplanting were similar to or exceeded those of pre-existed shoots, suggesting that the physiological status of transplants is similar to that of natural population after 7 months. Because the shell method did not require workers to be in the water, the method was cost and labor effective. Additionally, given that shells originate from marine environments, the shell method did not leave any hazardous materials in the transplanting areas after restoration.

Implementation of artificial neural networks (ANNs) to analysis of inter-taxa communities of benthic microorganisms and macroinvertebrates in a polluted stream.

This study was performed to gain an understanding of the structural and functional relationships between inter-taxa communities (macroinvertebrates as consumers, and microbes as decomposers or preys for the invertebrates) in a polluted stream using artificial neural networks techniques. Sediment samples, carrying microorganisms (eubacteria) and macroinvertebrates, were seasonally collected from similar habitats in streams with different levels of pollution. Microbial community taxa and densities were determined using polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE) and 16S rDNA sequence analysis techniques. The identity and density of macroinvertebrates were concurrently determined. In general, differences were observed on grouping by self-organizing map (SOM) in polluted, clean and recovering sites based on the microbial densities, while the community patterns were partly dependent on the sampling period. A Spearman rank order correlation analysis revealed correlations of several eubacterial species with those of macroinvertebrates: a negative correlation was observed between Acidovorax sp. (from polluted sites) and Gammaridae (mostly from the clean site), while Herbaspirillum sp. and Janthinobacterium sp. appeared to have positive correlations with some macroinvertebrate species. The population dynamics of the tolerant texa, Tubificidae and Chironomidae, appeared to be related with changes in the densities of Acidovorax sp. This study revealed community relationships between macroinvertebrates and microorganisms, reflecting the connectivity between the two communities via the food chain. A further physio-ecological and symbiological study on the invertebrate-microorganism relationships will be required to understand the degradation and utilization of detritus in aquatic ecosystems as well as to elucidate the roles of the inter-taxa in the recovery of polluted aquatic environments.

Site-specific success of three transplanting methods and the effect of planting time on the establishment of Zostera marina transplants.

Eelgrass, Zostera marina, is the most abundant seagrass species on the coast of Korea, but most large eelgrass meadows have disappeared since the 1970s due to human-induced disturbance. To restore disturbed seagrass habitats in die-off areas, seagrass transplanting has been attempted using various methods. Here, we assessed the feasibility and efficiency of seagrass transplanting methods depending on the sediment type at the planting site. Additionally, the effect of planting time on the establishment of transplant was examined to determine the optimal season for planting. We conducted an eelgrass transplanting experiment from fall 2003 to summer 2004 at three sites with different sediment types using three planting techniques. The staple method resulted in the highest transplant survival rate (77.1-93.8%) at all three sites, but was labor intensive. Transplanting Eelgrass Remotely with Frame Systems (TERFS) method also resulted in relatively a high survival rate (58.7-69.0%) at all sites. The shell method is a newer eelgrass transplanting method in which oyster shells are used as an anchoring device, and does not require SCUBA diving for subtidal transplanting. The shell method resulted in high survival rates in muddy (81.3%) and silty sediments (76.5%), but remarkably low survival rate in sandy sediments (5.0%). The TERFS, and shell methods reduced underwater labor; thus, these methods is suitable for large-scale seagrass restoration. Eelgrass transplants planted in summer had exhibited significant mortality due to high summer water temperatures. Although transplants planted in fall to spring had relatively high survival rates, transplanting and collection of vegetative shoots are difficult in winter and spring. Therefore, fall was suggested as the most effective transplanting season off the coast of Korea.