Sea urchin repelling Tannin– FeIII complex coating for ocean macroalgal afforestation
Graphical abstract
Graphical abstract: Schematic image showing the TA-FeIII complex coating on a target substrate and a possible repellent mechanism of the TA-FeIII complex.
Introduction
Macroalgal forests (kelp forests), a fertile habitat for a variety of marine organisms and a carbon dioxide sequestration site in marine ecosystems, have been disrupted off the coasts of east Asia, Australia, northern Europe, and north America due to climate change, ocean warming, and ocean acidification (Rosenzweig et al., 2008;Wernberg et al., 2012; Halpern et al., 2008). In addition, significant seaweed grazing by sea urchins and competition with calcified coralline algae have seriously disrupted the kelp forests (Steneck et al., 2002;Ling, 2009; Harrold and Pearse, 1987;Reed et al., 2006). Due to the negative effects of sea urchins and calcified coralline algae, these forests have been subsequently transformed into a barren land, and the restoration of these regions has become increasingly challenging (Wright et al., 2005;Gagnon et al., 2006). These areas are called urchin barrens because only sea urchins remain on a seafloor devoid of vegetation. Given the importance of the kelp forest to marine ecosystems, attempts to restore kelp forests have been made in America, Europe, Australia and Asia, but a practical solution relieving the damage of the urchin barrens has not been reported to date (Campbell et al., 2014;Galasso, 2015;Shear et al., 2012; Smith et al., 2004;Jung and Kim et al., 2020). Phlorotannin (Fig. 1b), a polyphenolic molecule secreted from most seaweed species, has been suggested as a repellent of marine herbivores, including the sea urchins. In recent decades, phlorotannin has exhibited deterrent effects to marine herbivory animals. Phlorotannin-containing extracts from brown algae inhibited sea urchin larval survival and reduced the appetites of marine herbivores, including sea urchins (Kubanek et al., 2004;Agatsuma, 2008; Shibata et al., 2014). It is hypothesized that its herbivore-repellent effect is due to its ability to bind to digestive enzymes in guts of the herbivores (Barbehenn and Constabel, 2011; Gustavson, 1954;Loomis and Battaile, 1965; Bernays, 1978). However, natural extraction of phlorotannin from seaweed is inefficient given the biomass required due to its low contents (3% (w/w) of dry weight of alginate (Shibata et al., 2002; Arnold and Targett, 2002). Consequently, tannin (TA) is suggested as a phlorotannin alternative because tannin is one of the most abundant and cost-effective polyphenolic compounds obtained from wood bark (Fig. 1a). Both TA and phlorotannin can be precipitated with digestive enzymes from herbivores, so the TA could exhibit herbivore-repellent effects. Recently, green- and cost-effective coatings on various types of target substrates using a Tannin- FeIII complex (TA-FeIII complex) were developed by exploiting a highly stable complex between metal ion/oxide and galloyl residues in tannin and have been applied to variety of biomedical and environmental applications (Zeng and Hwang et al., 2010; Ejima et al., 2013; Oh et al., 2015a). In this study, we report on a TA-Fe III coating used as a coating strategy for marine substrates and for the sustained release of tannin to repel sea urchins from kelp forests. The ability of the TA-FeIII coating to repel sea urchins was evaluated in both a model aquarium and an ocean field experiment.
Section snippets
Chemicals and collection of the sea urchins
Tannin powder from Chinese natural gall nuts, sodium alginate from brown algae and iron chloride(III) were purchased from Sigma-Aldrich (St. Louis, MO, USA). The seawater was collected from the Pohang coast region in Korea (36°9′2.54″N, 129°23′57.18″E), and the filtered seawater was prepared by filtering the collected seawater with a 0.45 μm filter (bottle-top vacuum filters, Corning, NY, USA). Both types of sea water have pH values of 8.1 and 34‰ salinity. The sodium alginate stock solution
Elution rate of TA-FeIII coating
To estimate and control the elution rate of the TA-FeIII eluates from the coating, an elution rate profile of the TA-FeIII coating was obtained using a UV–vis spectrophotometer. The absorbance values of 5, 10, 15, 20, 25, 30, and 50 μM TA-FeIII solution at 280 nm were 0.99, 0.134, 0.166, 0.199, 0.236, 0.284, and 0.471 respectively (Supplementary Material Fig. SM-1a). The absorbance values of the eluates from the TA-FeIII coating were 0.328, 0.333, 0.412, 0.414, 0.409, 0.439 and 0.453,
Conclusion
Given that the need for practical methods to repel sea urchins from kelp forests is increasing, we suggest Tannin -FeIII coating as a repellent agent against sea urchins based on the outstanding repelling effect of this agent against sea urchins as demonstrated using model aquarium and field experiments. Both the model aquarium and field experiments showed that the TA-FeIII coating has a deterrent effect against sea urchins, and we observed that the sea urchins responded to TA-FeIII content in
Credit author statement
Sinyang Kim and Sang Mok Jung conducted the model aquarium experiment, the elution rate measurement and field experiment and they wrote the original manuscript. Sungjune Jung advised and revised the manuscript Dong Soo Hwang and Hyun Woung Shin organized the whole work and revised the manuscript.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) [2016M1A5A1027592].
References (29)
- et al.
Tannins in plant–herbivore interactions
Phytochemistry
(2011) - et al.
Plant phenolic compounds and the isolation of plant enzymes
Phytochemistry
(1966) - et al.
Tunicate-mimetic nanofibrous hydrogel adhesive with improved wet adhesion
Acta Biomater.
(2015) - et al.
Inhibitory effect of 2, 4-dibromophenol and 2, 4, 6-tribromophenol on larval survival and metamorphosis of the sea urchin Strongylocentrotus nudus
Fish. Sci.
(2008) - et al.
Marine tannins: the importance of a mechanistic framework for predicting ecological roles
J. Chem. Ecol.
(2002) Tannins: an alternative viewpoint
Entomol. Exp. Appl.
(1978)- et al.
Towards restoration of missing underwater forests
PloS One
(2014) - et al.
Importance of iron for plankton blooms and carbon dioxide drawdown in the Southern Ocean
Nature
(1995) - et al.
One-step assembly of coordination complexes for versatile film and particle engineering
Science
(2013) - et al.
Temporal variation in community interfaces: kelp-bed boundary dynamics adjacent to persistent urchin barrens
Mar. Biol.
(2004)
Fish-seastar facilitation leads to algal forest restoration on protected rocky reefs
Sci. Rep.
Interaction of vegetable tannins with polyamides as proof of the dominant function of the peptide bond of collagen for its binding of tannins
J. Polym. Sci.
A global map of human impact on marine ecosystems
Science
The ecological role of echinoderms in kelp forests
Echinoderm Stud.
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These authors contributed equally to this work and should be considered as co-first authors.