A meta-analysis shows that seaweeds surpass plants, setting life-on-Earth’s limit for biomass packing

Abstract

BackgroundAs plants, algae and some sessile invertebrates may grow in nearly monospecific assemblies, their collective biomass increases and if they compete hard enough some die, freeing up space. The concurrent increase in biomass and decrease in density is called self-thinning, and its trajectory over time or maximum values represent a boundary condition. For a single stand developing over time the boundary defines the carrying capacity of the environment but the most extreme trajectories emulate the efficiency of species in packing biomass into space.ResultsHere we present a meta-analysis of compiled data on biomass and density from 56 studies of 42 species of seaweeds from 8 orders within 3 phyla scattered through the world’s oceans. Our analysis shows that, with respect to biomass, seaweeds are the most efficient space occupiers on Earth because they transgress previously fixed limits derived from land plants. This is probably because seaweeds are not limited by water and do not need structures for its transport or for transpiration; they photosynthesise and uptake nutrients over their entire surface; they are attached to the substrate by holdfasts that are small proportional to their volume or weight compared to roots; water provides them better support, reducing the need for tissues for rigidity. We also identified a biomass concentration common to plants and seaweeds which represents the threshold that no life on the planet can pass. Using each stand’s distance to the biomass–density boundary, we determined that within the seaweeds the efficiency of space occupation differed amongst taxonomic and functional groups as well as with clonality and latitude.ConclusionsAlgae occupy space more efficiently than plants, most likely because the watery environment facilitates the physical processes and integration of space occupation. The distance-to-the-boundary proves a good metric to discriminate among groups and may be useful for comparison of the most efficient biomass producing systems, or for the identification of systems impacted by pollution.Electronic supplementary materialThe online version of this article (10.1186/s12898-019-0218-z) contains supplementary material, which is available to authorized users.

A model for the biomass–density dynamics of seagrasses developed and calibrated on global data

“…This limitation is a consequence of our model being based on the biomass–density relation and Interspecific Boundary Line estimated from (and for) established stands. These fundamental ecological principles applied to terrestrial plants [19–21] and algae [22] are also only valid for established stands, and in the generality of the plant and algae cases the colonization of the free surface is by the dispersal of seedlings or sporelings instead of rhizome elongation. Seagrass stands that are not fully established require long term expansion of their rhizomes to fully occupy the free surfaces [14].…”

“…1). Above any self-thinning line is placed a boundary line that no stand or species can pass and reflects the maximum possible efficiency of space occupation [12, 20–22] (Fig. 1).…”

“…This boundary line is termed the Interspecific Boundary Line (IBL) and is given by log 10 B = β 0 + β 1 ∙log 10 D. The IBL for terrestrial plants has coefficients β 0 = 4.87 and β 1 = − 0.33 [21]. Recently, algae were demonstrated to occupy space more efficiently than plants [22], with the algae IBL exhibiting coefficients β 0 = 6.69 and β 1 = − 0.67 placed above the plant IBL (Fig. 1).…”

“…Nevertheless, there was a threshold of log 10 B ≈ 5 that neither algae nor plants were able to cross [22]. The perpendicular distance from each algal stand to their boundary reflected its specific efficiency of space occupation and was used to discriminate among taxa, functional groups, clonality or latitude [22]. Soon after, Vieira et al [12] demonstrated that seagrasses are also limited by their own IBL.…”

“…Self-thinning does not apply to many clonal algae and plants because modules (ramets) are physically interconnected allowing the sharing of acquired resources and offsetting competition [23–29]. Although not necessarily self-thinning, seagrasses [12], terrestrial clonal plants [23] and clonal algae [22] have been demonstrated to be limited by their respective IBL, as are non-clonal macrophytes. Therefore, it is both possible and legitimate to use their stands’ distances to their IBL as estimators of their efficiencies of space occupation.…”