Crustose coralline algae and associated microbial biofilms deter seaweed settlement on coral reefs

Abstract

Crustose coralline algae (CCA), a group of calcifying red algae found commonly in benthic marine ecosystems worldwide, perform essential ecological functions on coral reefs, including creating benthic substrate, stabilizing the reef structure and inducing coral settlement. An important feature of CCA is the ability to keep their surfaces free of epiphytic algae, thereby reducing algal overgrowth and allowing them access to light. However, the mechanisms by which CCA prevent settlement of opportunistic seaweeds (fleshy macroalgae) are not fully understood, nor is whether these mechanisms vary among CCA species. In our study based on the Great Barrier Reef, we demonstrate that three common CCA species (Titanoderma pustulatum, Porolithon onkodes and Neogoniolithon sp.) have a remarkable ability to deter settlement of seaweed spores. We provide experimental evidence that the CCA use allelopathy and microbial inhibition against the settlement of spores of the brown seaweed Padina boergesenii. Methanol extracts of allelopathic compounds from T. pustulatum, Po. onkodes and Neogoniolithon sp. significantly reduced the settlement of Pa. boergesenii spores by 4.3 times, 3.0 and 3.8 times, respectively. Further, we found that microbial biofilms, while having a lower inhibitory effect than allelopathic compounds, also reduced seaweed settlement of Pa. boergesenii. Our study demonstrates that allelopathy and microbial inhibition, in addition to epithallial tissue sloughing, are mechanisms employed by CCA to prevent the settlement of epiphytic algae. Understanding the mechanisms by which CCA avoid seaweed overgrowth contributes to our understanding of the dynamics of seaweed proliferations on reefs and to the ecological knowledge of this important group of reefbuilding organisms.

Influences of salinity on the physiology and distribution of the Arctic coralline algae, Lithothamnion glaciale (Corallinales, Rhodophyta)

“…, Kim et al. , Gomez‐Lemos and Diaz‐Pullido ). Interactions of this sort in polar habitats are not known, but organisms in the biofilm, or diffusion boundary layer, certainly contribute to the algal microenvironment (Hurd ).…”

“…Cues for abalone larvae have been identified from both corallines and their biofilm communities on temperate reefs (Daume et al 1999) and tropical reefs with coral larvae (Heyward and Negri 1999). Similarly, allelopathic compounds have been found in corallines and their biofilm communities, preventing the settlement and growth of other algal species in temperate and tropical systems (Suzuki et al 1998, Kim et al 2004, Gomez-Lemos and Diaz-Pullido 2017. Interactions of this sort in polar habitats are not known, but organisms in the biofilm, or diffusion boundary layer, certainly contribute to the algal microenvironment (Hurd 2000).…”

Species-Specific Differences in the Microbiomes and Organic Exudates of Crustose Coralline Algae Influence Bacterioplankton Communities

“…Moreover, research is showing that coral larvae have settlement preferences among different species of CCA (Harrington et al, 2004; Ritson-Williams et al, 2010, 2014), with some species of CCA facilitating and others inhibiting settlement for most of the coral species tested so far (Ritson-Williams et al, 2016). These preferential settlement patterns are possibly a result of the differing mechanisms by which CCA suppress the growth of opportunistic biofilms and macroalgae such as the production of secondary metabolites (Gomez-Lemos and Diaz-Pulido, 2017) and mechanical sloughing of epithelial tissue (Keats et al, 1997). Indeed, coral larval settlement studies have shown higher levels of sloughing and thus hazardous to larvae in Porolithon onkodes relative to other species of CCA such as Hydrolithon reinboldii and Titanoderma prototypum (Harrington et al, 2004).…”

Crustose coralline algae increased framework and diversity on ancient coral reefs

“…Since their appearance in the Early Cretaceous [ 6 ], CCA have developed an important, complicated relationship with corals. On modern coral reefs, CCA function as frame-builders and encrusting or binding organisms that stabilize reef accretion, prevent bioerosion, and induce settlement of coral and other invertebrate larvae ([ 4 , 7 , 8 , 9 , 10 ] and references therein).…”