Andrew J. Scardino

Mini review: Biomimetic models and bioinspired surfaces for fouling control.

Nature provides many examples of mechanisms to control fouling. These defences can be copied (biomimetic) or tailored (bioinspired) to solve problems of fouling on manmade structures. With increasing research in this area over the last two decades, it is timely to review this burgeoning subject, in particular as the biofouling field shifts focus towards novel, physical mechanisms to prevent and control fouling. This change is being promoted by advances in nano- and micro-scale patterning as well as in a variety of nano-biotechnologies, which are transforming the translation of natural surfaces into experimental materials. In this article, research on the defence of marine organisms against fouling and the technologies they are defining is reviewed.

Testing attachment point theory : diatom attachment on microtextured polyimide biomimics

Abstract This paper explores diatom attachment to a range of laser etched polyimide surfaces to directly test ‘attachment point theory’. Static bioassays were conducted on microtextured polyimide surfaces using four diatom species, Fallacia carpentariae, Nitzschia cf. paleacea, Amphora sp. and Navicula jeffreyi with cell sizes ranging from 1 – 14 μm. The microtextured polyimides were modelled from natural fouling resistant bivalve surfaces and had wavelengths above, below and at the same scale as the diatom cell sizes. Diatoms attached in significantly higher numbers to treatments where the numbers of attachment points was highest. The lowest diatom attachment occurred where cells were slightly larger than the microtexture wavelength, resulting in only two theoretical points of attachment. The results support attachment point theory and highlight the need to address larval/cell size in relation to the number of attachment points on a surface. Further studies examining a range of microtexture scales are needed to apply attachment point theory to a suite of fouling organisms and to develop structured surfaces to control the attachment and development of fouling communities.

The role of nano-roughness in antifouling

Nano-engineered superhydrophobic surfaces have been investigated for potential fouling resistance properties. Integrating hydrophobic materials with nanoscale roughness generates surfaces with superhydrophobicity that have water contact angles (θ) >150° and concomitant low hysteresis (<10°). Three superhydrophobic coatings (SHCs) differing in their chemical composition and architecture were tested against major fouling species (Amphora sp., Ulva rigida, Polysiphonia sphaerocarpa, Bugula neritina, Amphibalanus amphitrite) in settlement assays. The SHC which had nanoscale roughness alone (SHC 3) deterred the settlement of all the tested fouling organisms, compared to selective settlement on the SHCs with nano- and micro-scale architectures. The presence of air incursions or nanobubbles at the interface of the SHCs when immersed was characterized using small angle X-ray scattering, a technique sensitive to local changes in electron density contrast resulting from partial or complete wetting of a rough interface. The coating with broad spectrum antifouling properties (SHC 3) had a noticeably larger amount of unwetted interface when immersed, likely due to the comparatively high work of adhesion (60.77 mJ m−2 for SHC 3 compared to 5.78 mJ m−2 for the other two SHCs) required for creating solid/liquid interface from the solid/vapour interface. This is the first example of a non-toxic, fouling resistant surface against a broad spectrum of fouling organisms ranging from plant cells and non-motile spores, to complex invertebrate larvae with highly selective sensory mechanisms. The only physical property differentiating the immersed surfaces is the nano-architectured roughness which supports longer standing air incursions providing a novel non-toxic broad spectrum mechanism for the prevention of biofouling.

Attachment point theory revisited: the fouling response to a microtextured matrix

This paper examines attachment point theory in detail by testing the fouling attachment of several fouling groups to a microtextured matrix. Static bioassays were conducted on polycarbonate plates with nine equal regions, comprising eight scales of microtexture (4–512 µm) and one untextured region. The microtextures examined were continuous sinusoidal ridges and troughs of defined height and width. Attachment over the microtextured plates was examined for the diatom Amphora sp., the green alga Ulva rigida, the red alga Centroceras clavulatum, the serpulid tube worm Hydroides elegans and the bryozoan Bugula neritina. It was found that the size of the microtexture in relation to the size of the settling propagules/larvae was important in the selection of attachment sites. Attachment was generally lower when the microtexture wavelength was slightly smaller than the width of the settling propagules/larvae and increased when the wavelength was wider than their width. The effect of attachment points was weak for small motile microfoulers (Amphora sp. and U. rigida) (7 µm), strong for large macrofouling larvae (H. elegans and B. neritina) (129–321 µm) and non-existent for the non-motile algal spores (C. clavulatum) (37 µm). This study reinforces the potential of using attachment points to develop surfaces with increased fouling resistance or, alternatively, surfaces which promote the attachment of selected target sizes of motile propagules or larvae.

Microtopography and antifouling properties of the shell surface of the bivalve molluscs mytilus galloprovincialis and pinctada imbricata

Biofouling rapidly covers most submerged surfaces in the marine environment. However, some marine organisms remain clean despite strong fouling pressure. Potential physical inhibitors of fouling were investigated by comparing the thickness, cover, and microtopographic structure of the periostracum of two bivalve molluscs, the blue mussel, Mytilus galloprovincialis , and the pearl oyster, Pinctada imbricata . The cover and thickness of the periostracum were measured on four size classes of each species using histological and microscopic techniques. The periostracum of M. galloprovincialis was significantly thicker than that of P. imbricata and did not differ significantly between size classes. In contrast, the periostracum of P. imbricata decreased significantly with increasing size in both thickness and cover. The microtopography of the shell surface of both species was measured using atomic force microscopy (AFM) and scanning electron microscopy (SEM), which revealed a homogeneous ridged surface for M. galloprovincialis with a uniform distance of 1-2 w m between ridges with a mean depth of 1.5 w m. P. imbricata had a heterogeneous surface structure without a repeating structural pattern. To compare the potential antifouling properties of the shell surface the four size classes of both species were tested in fourteen-week field exposure trials. M. galloprovincialis was rarely fouled over the trial period with less than 10% of M. galloprovincialis shell across all size classes being fouled. In contrast, P. imbricata had significantly higher levels of fouling. Both the proportion of P. imbricata shells fouled and the density of fouling organisms were positively correlated with the age of the shell and the amount of intact periostracum. The relationship between the shell surface microtopography and the intensity of fouling is discussed.

Attachment strength is a key factor in the selection of surfaces by barnacle cyprids (Balanus amphitrite) during settlement.

This manuscript constitutes the first evidence of the effects of texture on the rate of removal of cyprids from surfaces and the link between settlement preferences and susceptibility to removal by force. Cyprids of Balanus amphitrite settled preferentially on sinusoidal linear textures (1:1 aspect ratio) in the range 0–32 μm, with textures on the scale of the cyprid (512 μm) treated as flat. Polycarbonate was preferred as a substratum to a polydimethylsiloxane (PDMS) elastomer. Textures of 64–256 μm were avoided and the texture of 256 μm in PDMS was the least preferred substratum tested, with no settlement of cyprids. Hydrodynamic removal was inversely correlated to settlement rate on the textures assayed, implying an adaptive response by cyprids to select surface textures to which their attachment was most tenacious. Correlation plots suggest that likelihood of removal by force is not the only factor involved when cyprids elect to settle on a given texture. Choice and no-choice assays delivered different results. This discrepancy is partially ascribed to inherent variability in the choice assay method, but also to the ability of cyprids to compare textures and exercise true choice, biasing settlement towards stimulatory textures in preference to intermediate textures that were settled on in the absence of choice. The identification of a link between settlement preference and likelihood of removal will assist practically in the development of fouling-resistant marine coatings.

Fouling deterrence on the bivalve shell Mytilus galloprovincialis: a physical phenomenon?

The physical nature of fouling deterrence by the mussel Mytilus galloprovincialis was investigated using high-resolution biomimics of the bivalve surface. The homogeneous microtextured surface of M. galloprovincialis (1.94 ± 0.03 μm), the smooth surface of the bivalve Amusium balloti (0 μm), and moulds of these surfaces (biomimics) were compared with controls of smooth (0 μm) and sanded moulds, (55.4 ± 2.7 μm) and PVC strips (0 μm) in a 12-week field trial. The shell and mould of M. galloprovincialis were fouled by significantly fewer species and had significantly less total fouling cover than the shell and mould of A. balloti over a 12-week period. However, the major effects were between surfaces with and without microtopography. Surface microtopography, be it structured as in the case of M. galloprovincialis shell and mould, or random as in the case of the sanded mould, had a lower cover of fouling organisms than treatments without microtopography after 6 weeks. There was also no difference between the effect of the M. galloprovincialis mould and the sanded mould. The strong fouling deterrent effects of both these surfaces diminished rapidly after 6 to 8 weeks while that of M. galloprovincialis shell remained intact for the duration of the experiment suggesting factors in addition to surface microtopography contribute to fouling deterrence.

Biomimetic characterisation of key surface parameters for the development of fouling resistant materials.

Material science provides a direct route to developing a new generation of non-toxic, surface effect-based antifouling technologies with applications ranging from biomedical science to marine transport. The surface topography of materials directly affects fouling resistance and fouling removal, the two key mechanisms for antifouling technologies. However, the field is hindered by the lack of quantified surface characteristics to guide the development of new antifouling materials. Using a biomimetic approach, key surface parameters are defined and quantified and correlated with fouling resistance and fouling removal from the shells of marine molluscs. Laser scanning confocal microscopy was used to acquire images for quantitative surface characterisation using three-dimensional surface parameters, and field assays correlated these with fouling resistance and fouling release. Principle component analysis produced a major component (explaining 54% of total variation between shell surfaces) that correlated with fouling resistance. The five surface parameters positively correlated to increased fouling resistance were, in order of importance, low fractal dimension, high skewness of both the roughness and waviness profiles, higher values of isotropy and lower values of mean surface roughness. The second component (accounting for 20% of variation between shells) positively correlated to fouling release, for which higher values of mean waviness almost exclusively dictated this relationship. This study provides quantified surface parameters to guide the development of new materials with surface properties that confer fouling resistance and release.

Functional morphology of scale hinges used to transport water: convergent drinking adaptations in desert lizards ( Moloch horridus and Phrynosoma cornutum )

The Australian thorny devil, Moloch horridus Gray, 1841, and the Texas horned lizard, Phrynosoma cornutum Harlan, 1825, have the remarkable ability to rapidly move water through interscalar spaces on their skin’s surface to their mouth for drinking. The morphology of these scale hinges has not been studied. We used histological and SEM techniques to examine and compare the scale hinges of both species. Additional taxa in their respective lineages were examined in order to evaluate the potential that convergent evolution has occurred. In the two species that transport water, each scale hinge has a basally expanded and semi-enclosed channel formed by the hinge joint that is interconnected with all scale hinges on the body. We hypothesize that it is within this semi-tubular channel system of hinge joints, where the β-layer keratin of the integument is very thin, that water is transported. Hinge joint walls are covered by a complex topography of fractured surfaces that greatly expand the channel’s surface area and probably enhance capillary transport of water. In addition, we note differing morphology of scale surfaces at the rear of the jaws of both species. We hypothesize that capillary forces fill the scale-hinge system and additional forces, generated within the mouth by observed motions during drinking, depress local water-pressure to pull water through the channels of the hinge-joint system. We conclude that the combined features in the two species, semi-tubular hinge-joint channels with convoluted walls and a jaw-buccal cavity pumping-mechanism, have convergently evolved for capture, transport, and drinking of water from sporadic rainfall.

Relevance of mytilid shell microtopographies for fouling defence - a global comparison

Prevention of epibiosis is of vital importance for most aquatic organisms, which can have consequences for their ability to invade new areas. Surface microtopography of the shell periostracum has been shown to have antifouling properties for mytilid mussels, and the topography shows regional differences. This article examines whether an optimal shell design exists and evaluates the degree to which shell microstructure is matched with the properties of the local fouling community. Biomimics of four mytilid species from different regional provenances were exposed at eight different sites in both northern and southern hemispheres. Tendencies of the microtopography to both inhibit and facilitate fouling were detected after 3 and 6 weeks of immersion. However, on a global scale, all microtopographies failed to prevent fouling in a consistent manner when exposed to various fouling communities and when decoupled from other shell properties. It is therefore suggested that the recently discovered chemical anti-microfouling properties of the periostracum complement the anti-macrofouling defence offered by shell microtopography. 1Laboratório de Manejo, Ecologia e Conservação Marinha, Instituto Oceanográfico, Universidade de São Paulo, Praça do Oceanográfico, 191, CEP 05508-900, São Paulo - SP, Brazil. 2ARONIA Coastal Zone Research Team, Novia University of Applied Sciences at Åbo akademi, Raserborgvägen 9, Ekenäs, Finland. 3Marine Science and Fisheries Department, College of Agricultural and Marine Sciences, Sultan Qaboos University, Al-Khoud, PO Box 34, 123 Muscat, Sultanate of Oman. 4CEAZA – Centro de Estudios Avancados en Zonas Aridas, Universidad Católica del Norte, Larrondo 1281, Coquimbo, Chile. 5Maritime Platforms Division, Defence Science & Technology Organisation, 506 Lorimer Street, Fishermans Bend, Vic 3207, Australia. 6Natural England, North East Region, The Quadrant, Newburn Riverside, Newcastle upon Tyne NE15 8NZ, UK.