Restoration of seagrass habitat leads to rapid recovery of coastal ecosystem services

There have been increasing attempts to reverse habitat degradation through active restoration, but few largescale successes are reported to guide these efforts. Here, we report outcomes from a unique and very successful seagrass restoration project: Since 1999, over 70 million seeds of a marine angiosperm, eelgrass (Zostera marina), have been broadcast into mid-western Atlantic coastal lagoons, leading to recovery of 3612 ha of seagrass. Well-developed meadows now foster productive and diverse animal communities, sequester substantial stocks of carbon and nitrogen, and have prompted a parallel restoration for bay scallops (Argopecten irradians). Restored ecosystem services are approaching historic levels, but we also note that managers value services differently today than they did nine decades ago, emphasizing regulating in addition to provisioning services. Thus, this study serves as a blueprint for restoring and maintaining healthy ecosystems to safeguard multiple benefits, including co-benefits that may emerge as management priorities over time

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

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

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 370 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 simple 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 intensity, but also insight into the mechanisms that relate temperature and biogeographic gradients in species interactions

Attributes of seaweeds and seagrasses that may influence seaweed impact on seagrass.

<p>We had <i>a priori</i> expectations about the direction of impact for the first seven attributes (above the dotted line). These directional hypotheses are based on simple rules; we expect a large impact when there is (a) <i>more</i> of a stressor (the seaweed) in either space or time, or (b) <i>less</i> of the impacted organism (the seagrass). Summary of tests-results are shown in the table (significant values in bold, see also <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028595#pone-0028595-g001" target="_blank">Fig. 1</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028595#pone-0028595-g002" target="_blank">2</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028595#pone.0028595.s007" target="_blank">Appendix S3</a>; NT = not tested because data were inadequate).</p>1<p>Impact of seaweeds on seagrasses may also be modified by habitat attributes, including the resource levels (e.g., nutrients, light, O₂, space), abiotic conditions (e.g., temperature, salinity, desiccation, sedimentation, substrate conditions, day-length) and resident animals living in and around the seagrass habitat <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028595#pone.0028595-Thomsen1" target="_blank">[21]</a>.</p>2<p>The categorical test based on experiments that explicitly tested for abundance effect was significant, but the correlation conducted across all experiments was not significant.</p>3<p>We assume that abundant seagrasses have more resources to withstand stress. Alternatively, abundant seagrass may suffer from intra-specific competition resulting in abundant seagrass being more susceptible to stress (i.e. the opposite expectation may be equally valid).</p>4<p>We assume that invaders have superior impact (seaweeds) and resistance (seagrass), e.g., as novel weapons <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028595#pone.0028595-Catford1" target="_blank">[44]</a>.</p>5<p>Poor ‘condition/health’ of the seaweed results in decomposition and production of anoxia, sulphide and ammonia. Unattached mats often decompose when lower layers are shaded by higher layers.</p>6<p>For seagrasses, integration is a continuous attribute that encompasses below ground storage products and ability to translocate products between ramets.</p>7<p>Dri = Drift/unattached, Epi = epiphytic to seagrass leaves, Roo = rooted in sediment with rhizoids and rhizomes.</p>8<p>A few seagrasses can attach to rocks, but no studies have quantified seaweed impacts on attached seagrass.</p>9<p>Adapted from Littler and Littler (1980); She = sheets, Coa = Coarsely branches, Fil = filaments, Coe = coenocytic.</p>10<p>Ulv = <i>Ulva</i>, Gra = <i>Gracilaria</i>, Lau = <i>Laurencia</i>, Cau = <i>Caulerpa.</i></p>11<p>Amp = <i>Amphibolis</i>, Tha = <i>Thalassia</i>, Cym = <i>Cymodocea</i>, Zos = <i>Zostera</i>, Had = <i>Halodule</i>, Hap = <i>Halophila</i>.</p

Effects of seaweed attributes on seagrass performance.

<p>Hedges <i>d</i> represent <i>d</i>_experiment for continuous data and <i>d</i>_cumulative ±95% CL for categorical data. Data were extracted from up to 59 experiments. Fig. B is based on 17 experiments that tested explicitly for abundance effects. Effects are here reported as Δ<i>d</i> = <i>d</i>_high−<i>d</i>_low; if Δ<i>d</i> is negative then high abundance cause larger negative effect than low abundance. Fig. G: coenocytic = single celled seaweed with modular growth of interconnected fronds. For meta-analytical test results and sample sizes, see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028595#pone.0028595.s007" target="_blank">Appendix S3</a>.</p

Modifying effects of seagrass attributes on seaweed impacts.

<p>Hedges <i>d</i> represent <i>d</i>_experiment for continuous and <i>d</i>_cumulative ±95% CL for categorical data. Data were extracted from up to 59 experiments. For meta-analytical test results and sample sizes, see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028595#pone.0028595.s007" target="_blank">Appendix S3</a>.</p

Seaweed impacts on seagrasses can be partially predicted from basic impact attributes.

<p><i>Plot 3A: Key meta-analytical results schematized</i> (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028595#pone-0028595-g001" target="_blank">Fig. 1</a>–<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028595#pone-0028595-g002" target="_blank">2</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028595#pone-0028595-t001" target="_blank">Table 1</a>). Impact depends on <u>seaweed abundance</u> (low <i>vs.</i> high, cf. y-axis), <u>seaweed attachment</u> (unattached <i>vs.</i> epiphytic <i>vs.</i> rooted, cf. long x-axis) and <u>seagrass size</u> (large <i>vs.</i> small, cf. short x-axis). The impact mechanisms associated with seaweed abundance and seagrass size are simple; the more of the stressor (seaweed) and less of the impacted organism (seagrass) the larger the impact. The mechanisms that cause different effects between attachment types are less obvious; we suggest that oxygen and light reduction and sulphide production cause large negative impact of unattached and epiphytic seaweeds, whereas allelochemicals cause smaller impacts of rooted seaweeds (listed in bullets). Our analysis addressed impact attributes in isolation. Future tests should use factorial designs to identify interactions between attributes. <i>Plot 3B: Figure legend</i>. Standardized seagrass = three green leaves connected with rhizomes; leaves can be large or small. Standardized seaweed = brown frond; can be sparse or abundant (1 <i>vs.</i> 3 fronds), positioned vertical (attached <i>vs.</i> rooted) or horizontal (unattached), and with (rooted) or without (unattached, attached) inter-connecting rhizome. <i>Plot 3C: Non-impacted controls.</i> The impact treatments shown in plot 3A should always be compared to non-impacted seagrass controls, here to ‘large and small seagrass without seaweed stress’.</p