Influences of biofilm-associated ciliates on the settlement of marine invertebrate larvae

Abstract

Settlement of benthic marine invertebrate larvae often limits recruitment, influencing the structure and dynamics of natural populations as well as biofouling of marine infrastructure, ship hulls, and aquaculture operations. Certain microbial components of substratum biofilms influence settlement (e.g. bacteria, diatoms), but the importance of biofilm protozoa has been unknown. We tested for effects of ciliates by comparing settlement and survival of common fouling invertebrates among 3 biofilm conditions: no biofilm, a purely bac terial biofilm, and a biofilm of bacteria and ciliates. With an assemblage of 7 ciliates (from Hypotrichia, Haptoria, and Scuticociliatia), the serpulid polychaete Galeolaria caespitosa showed a 44 to 49% average reduction in settlement rate compared to the purely bacterial biofilm, and post-settlement mortality increased 7-fold to 34%. In contrast, settlement and survival of the bryozoan Bugula neritina were unaffected. With a partially different assemblage of 11 ciliates (from Hypotrichia, Sticho trichia, Haptoria, Colpodida, and Scuticociliatia), settle ment of the serpulid Pomatoceros taeniata more than doubled, whereas that of the blue mussel Mytilus galloprovincialis was reduced by 54% compared to the purely bacterial biofilm. The results could not be explained by ciliates changing the total abundance of biofilm bacteria. We hypothesize that mechanisms could include direct interactions between larvae and ciliates (physical interactions, interference from ciliates' feeding currents, or responses to chemicals from ciliates), or indirect effects from ciliates altering the bacterial assemblage or its settlement cues. Such large and species-specific effects of ciliates on larval settlement and postsettlement mortality might impact invertebrate recruitment rates and species assemblages, especially because biofilm ciliates are highly variable over time and space.Aggregation of the tubeworm Galeolaria caespitosa. Larval settlement of these and other invertebrates is influenced by ciliates on the substratum.

Recruitment of the Pacific oyster Crassostrea gigas in a shellfish-exploited Mediterranean lagoon: discovery, driving factors and a favorable environmental window

“…Picoplankton also support grazing by ciliate and flagellate protists (Lam-Hoai et al 1997, Bec et al (Plunket & Hidu 1978, Elston et al 1999, Shimeta et al 2012. Our results support this hypothesis since a negative correlation was observed between the abundance of ciliates and the metamorphosis success of C. gigas.…”

Phytoplankton growth inhibited by the toxic and bacterivorous ciliate Uronema marinum (Protozoa, Ciliophora)

“…When Uronema marinum grow in biofilms, dispersion of its toxin may be relatively low compared to a pelagic environment (Shimeta et al 2012). This means that in future ecological laboratory studies of U. marinum and its toxin a distinction should be made between pelagic and benthic or biofilm habitats.…”

“…For instance, the settlement of the tube worm Galeolaria caespitosa and the blue mussel Mytilus galloprovincialis was significantly reduced by the presence of bacteria and ciliates compared to the presence of a pure bacterial biofilm (Shimeta et al 2012). Uronema mari num was part of the biofilm assemblage and it can be speculated that its toxins produced the negative effects on larval settlement and post-settlement mortality.…”

“…In a recent study, Shimeta et al (2012) discovered that biofilm associated ciliates had a variety of effects on the settlement of marine invertebrate larvae. For instance, the settlement of the tube worm Galeolaria caespitosa and the blue mussel Mytilus galloprovincialis was significantly reduced by the presence of bacteria and ciliates compared to the presence of a pure bacterial biofilm (Shimeta et al 2012).…”

“…Bacterial abundances in sea water generally lie between 10 5 and 10 7 cells ml −1 , which is similar to bacterial concentrations reached in this study. Therefore, in the present study, the abundances of U. marinum and bacteria, as well as the ciliate's growth rate, were comparable to data obtained in field studies.When Uronema marinum grow in biofilms, dispersion of its toxin may be relatively low compared to a pelagic environment (Shimeta et al 2012). This means that in future ecological laboratory studies of U. marinum and its toxin a distinction should be made between pelagic and benthic or biofilm habitats.…”