Sea urchin repelling Tannin– Fe^III complex coating for ocean macroalgal afforestation

Highlights

• TA-Fe^III coating on marine substrate is a practical solution for urchin barren.

• Tannin-Fe^III coating exhibited the ability to repel sea urchins.

• Sea urchin avoidance responses were positively related to the TA-Fe^III concentration.

• The repelling ability of Tannin-Fe^III was also evident in ocean filed experiments.

Abstract

Intense seaweed grazing by sea urchins has destroyed kelp forests and accelerated the transformation of these forests into barren areas known as urchin barrens. Once the sea urchins occupy the barren ground, it becomes more challenging to restore the kelp forests. Although phlorotannin, a primary herbivore defense chemical secreted by kelp, has been reported to discourage feeding activities of marine herbivores but the direct application of naturally extracted phlorotannin does not effectively repel sea urchins. In this study, we applied a simple and green Tannin-Fe^III (TA-Fe^III) coating on substrates as a sea urchin repellent using a cheap, ecofriendly tannin (TA) obtained from biomass as an alternative to phlorotannin. In a model aquarium experiment, most of the sea urchins (Anthocidaris crassispina) in the tank evaded the TA-Fe^III-coated substrates. In field tests with 300 sea urchins, the majority of sea urchins could not crawl over the TA-Fe^III-coated rope for more than 2 h in contrast to the control group. Hence, the safety, cost-effectiveness, and scalability of the TA-Fe^III coating make it a practical candidate to protect the kelp ecosystem from sea urchins.

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- Fe^III complex (TA-Fe^III 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-Fe^III coating to repel sea urchins was evaluated in both a model aquarium and an ocean field experiment.