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

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

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

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