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.

[1]  Jan Genzer,et al.  Development and testing of hierarchically wrinkled coatings for marine antifouling. , 2009, ACS applied materials & interfaces.

[2]  T. Norton,et al.  Settlement and survival of epiphytes on two intertidal crustose coralline alga , 1997 .

[3]  J. Davenport,et al.  Antifouling performance of the embryo and eggcase of the dogfish Scyliorhinus canicula , 1994 .

[4]  A J Scardino,et al.  Testing attachment point theory: diatom attachment on microtextured polyimide biomimics , 2006, Biofouling.

[5]  M. Thiel,et al.  Relevance of mytilid shell microtopographies for fouling defence – a global comparison , 2010, Biofouling.

[6]  M. Hermansson,et al.  Chemical inhibition of bacterial colonization by the red alga Bonnemaisonia hamifera , 2005 .

[7]  Martin Wahl,et al.  The Influence of Natural Surface Microtopographies on Fouling , 2004, Biofouling.

[8]  H. Erbil,et al.  Transformation of a Simple Plastic into a Superhydrophobic Surface , 2003, Science.

[9]  V. Paul,et al.  Mini-review: quorum sensing in the marine environment and its relationship to biofouling , 2009, Biofouling.

[10]  J. Mckenzie,et al.  The echinoderm surface and its role in preventing microfouling. , 1996, Biofouling.

[11]  D. J. Cookson,et al.  The role of nano-roughness in antifouling , 2009, Biofouling.

[12]  J. Hills,et al.  Settlement of barnacle larvae is governed by Euclidean and not fractal surface characteristics , 1999 .

[13]  H. Pavia,et al.  Chemical versus mechanical inhibition of fouling in the red alga Dilsea carnosa , 2005 .

[14]  C. Werner,et al.  Antifouling potential of Subtilisin A immobilized onto maleic anhydride copolymer thin films , 2009, Biofouling.

[15]  Adam W Feinberg,et al.  Engineered antifouling microtopographies – effect of feature size, geometry, and roughness on settlement of zoospores of the green alga Ulva , 2007, Biofouling.

[16]  R. Nys,et al.  Localisation and surface quantification of secondary metabolites in the red alga Delisea pulchra , 1999 .

[17]  P. Jonsson,et al.  Rejection of unsuitable substrata as a potential driver of aggregated settlement in the barnacle Balanus improvisus , 2004 .

[18]  R. Nys,et al.  Biomimetic characterisation of key surface parameters for the development of fouling resistant materials , 2009, Biofouling.

[19]  M. Úriz.  Mineral skeletogenesis in sponges , 2006 .

[20]  R E Baier,et al.  Adhesion: mechanisms that assist or impede it. , 1968, Science.

[21]  Robert F. Madgic.  A Model , 1981 .

[22]  Geoffrey Swain,et al.  Bioinspiration—the solution for biofouling control? , 2009, Bioinspiration & biomimetics.

[23]  Rocky de Nys,et al.  Fouling Deterrence on the Bivalve Shell Mytilus galloprovincialis: A Physical Phenomenon? , 2004, Biofouling.

[24]  Ying Xu,et al.  Natural products as antifouling compounds: recent progress and future perspectives , 2009, Biofouling.

[25]  Christopher J. Long,et al.  A model that predicts the attachment behavior of Ulva linza zoospores on surface topography , 2010, Biofouling.

[26]  Nick Aldred,et al.  Species-specific engineered antifouling topographies: correlations between the settlement of algal zoospores and barnacle cyprids , 2007, Biofouling.

[27]  Wilfried Meyer,et al.  Average nanorough skin surface of the pilot whale (Globicephalamelas, Delphinidae): considerations on the self-cleaning abilities based on nanoroughness , 2002 .

[28]  B. Chisholm,et al.  New Directions in Antifouling Technology , 2010 .

[29]  J. Mckenzie,et al.  Comparative study of sub-cuticular bacteria in brittlestars (Echinodermata: Ophiuroidea) , 1994, Marine Biology.

[30]  J. Kacza,et al.  Surface Properties of the Skin of the Pilot Whale Globicephala melas , 2003, Biofouling.

[31]  A. Brennan,et al.  Non-toxic antifouling strategies , 2010 .

[32]  F. Weinberger.  Pathogen-Induced Defense and Innate Immunity in Macroalgae , 2007, The Biological Bulletin.

[33]  S. Kjelleberg,et al.  Chemical mediation of bacterial surface colonisation by secondary metabolites from the red alga Delisea pulchra , 1998 .

[34]  R. Nys,et al.  Cost of chemical defence in the red alga Delisea pulchra , 2006 .

[35]  Xuefeng Gao,et al.  Biophysics: Water-repellent legs of water striders , 2004, Nature.

[36]  R. Nys,et al.  The effect of age and shell size on accumulation of fouling organisms on the Akoya pearl oyster Pinctada fucata (Gould) , 2006 .

[37]  R. de Nys,et al.  Surface microtopographies of tropical sea stars: lack of an efficient physical defence mechanism against fouling , 2007, Biofouling.

[38]  Peter D. Steinberg,et al.  Broad spectrum effects of secondary metabolites from the red alga delisea pulchra in antifouling assays , 1995 .

[39]  L. Mahadevan,et al.  Nested self-similar wrinkling patterns in skins , 2005, Nature materials.

[40]  T. Charlton,et al.  Quantitative variation of secondary metabolites in the sea hare Aplysia parvula and its host plant, Delisea pulchra , 1996 .

[41]  J. Mckenzie,et al.  Carbodiimide-induced labelling of sea urchin surfaces (Echinoidea, Echinodermata) , 1995 .

[42]  P. Gatenholm,et al.  Reduction of barnacle recruitment on micro‐textured surfaces: Analysis of effective topographic characteristics and evaluation of skin friction , 2000 .

[43]  J. Thomason,et al.  A comparative study of the anti-settlement properties of mytilid shells , 2006, Biology Letters.

[44]  M. Hermansson,et al.  Seaweed defence against bacteria: a poly-brominated 2-heptanone from the red alga Bonnemaisonia hamifera inhibits bacterial colonisation , 2008 .

[45]  A. Scardino.  Surface modification approaches to control marine biofouling , 2009 .

[46]  R. Nys,et al.  Pedicellariae of the crown-of-thorns sea star Acanthaster planci are not an effective defence against fouling , 2007 .

[47]  Jin Zhai,et al.  Super-hydrophobic surfaces: From natural to artificial , 2002 .

[48]  D. McDougald,et al.  The use of quorum-sensing blockers as therapeutic agents for the control of biofilm-associated infections. , 2005, Current opinion in investigational drugs.

[49]  Sheelagh L. Conlan,et al.  The effects of a serine protease, Alcalase®, on the adhesives of barnacle cyprids (Balanus amphitrite) , 2008, Biofouling.

[50]  A. Warén,et al.  Fouling-resistant surfaces of tropical sea stars , 2007, Biofouling.

[51]  Rodolfo E. Pérez-Roa,et al.  Involvement of reactive oxygen species in the electrochemical inhibition of barnacle (Amphibalanus amphitrite) settlement , 2009, Biofouling.

[52]  Abraham Marmur,et al.  Super-hydrophobicity fundamentals: implications to biofouling prevention , 2006, Biofouling.

[53]  S. Kjelleberg,et al.  Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling , 1996, Journal of bacteriology.

[54]  L Ploux,et al.  The interaction of cells and bacteria with surfaces structured at the nanometre scale. , 2010, Acta biomaterialia.

[55]  Martin Wahl,et al.  Non‐toxic protection against epibiosis , 1998 .

[56]  P. Steinberg,et al.  Linking marine biology and biotechnology. , 2002, Current opinion in biotechnology.

[57]  M. Hadfield,et al.  Effects of initial surface wettability on biofilm formation and subsequent settlement of Hydroides elegans , 2009, Biofouling.

[58]  D. Siebers,et al.  A zymogel enhances the self-cleaning abilities of the skin of the pilot whale (Globicephala melas). , 2001, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[59]  H. Pavia,et al.  Chemical settlement inhibition versus post-settlement mortality as an explanation for differential fouling of two congeneric seaweeds , 2003, Oecologia.

[60]  N. Lindquist,et al.  Constraints on Chemically Mediated Coevolution: Multiple Functions for Seaweed Secondary Metabolites , 1995 .

[61]  M. Hermansson,et al.  The red alga Bonnemaisonia asparagoides regulates epiphytic bacterial abundance and community composition by chemical defence. , 2010, FEMS microbiology ecology.

[62]  Christopher J. Long,et al.  Engineered antifouling microtopographies: mapping preferential and inhibitory microenvironments for zoospore attachment , 2010, Biofouling.

[63]  S. Golubić,et al.  Biodegradation of shells of the black pearl oyster, Pinctada margaritifera var. cumingii, by microborers and sponges of French Polynesia , 1996 .

[64]  E. Harper,et al.  A defensive value of the thickened periostracum in the Mytiloidea , 1993 .

[65]  Barbara Mulloy,et al.  Anti-adhesive glycoproteins in echinoderm mucus secretions. , 2004, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[66]  Lei Jiang,et al.  Bioinspired surfaces with special wettability. , 2005, Accounts of chemical research.

[67]  J. Mckenzie,et al.  Survey of the occurrence and morphology of sub-cuticular bacteria in shelf echinoderms from the north-east Atlantic Ocean , 1995 .

[68]  Nick Aldred,et al.  Attachment strength is a key factor in the selection of surfaces by barnacle cyprids (Balanus amphitrite) during settlement , 2010, Biofouling.

[69]  R. Lamb,et al.  Engineering nanoscale roughness on hydrophobic surface—preliminary assessment of fouling behaviour , 2005 .

[70]  Wolfram Hage,et al.  Experiments with three-dimensional riblets as an idealized model of shark skin , 2000 .

[71]  B. Dunn,et al.  Bioinspired living skins for fouling mitigation , 2009 .

[72]  Maureen E. Callow,et al.  Microtopographic Cues for Settlement of Zoospores of the Green Fouling Alga Enteromorpha , 2002 .

[73]  R. Nys,et al.  Attachment point theory revisited: the fouling response to a microtextured matrix , 2008, Biofouling.

[74]  W. O'Connor,et al.  Microtopography and antifouling properties of the shell surface of the bivalve molluscs mytilus galloprovincialis and pinctada imbricata , 2003, Biofouling.

[75]  Christopher J. Long,et al.  Engineered antifouling microtopographies: the role of Reynolds number in a model that predicts attachment of zoospores of Ulva and cells of Cobetia marina , 2010, Biofouling.

[76]  Jing Wang,et al.  Artifical fish flocked surface as a possible anti-biofoulant , 2009, 2009 4th IEEE International Conference on Nano/Micro Engineered and Molecular Systems.

[77]  C. Amsler,et al.  A New Antifouling Bioassay Monitoring Brown Algal Spore Swimming Behaviour in the Presence of Echinoderm Extracts , 2003, Biofouling.

[78]  R. Nys,et al.  Chemical defence against bacteria in the red alga Asparagopsis armata: linking structure with function , 2006 .

[79]  Christopher J. Long,et al.  Potential for tunable static and dynamic contact angle anisotropy on gradient microscale patterned topographies. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[80]  Jan Genzer,et al.  Recent developments in superhydrophobic surfaces and their relevance to marine fouling: a review , 2006, Biofouling.

[81]  Robert E. Baier,et al.  Surface characterisation of two gorgonian coral species: Implications for a natural antifouling defence , 1990 .

[82]  Diego Meseguer Yebra,et al.  Advances in marine antifouling coatings and technologies , 2009 .

[83]  John Davenport,et al.  Antibacterial and Antisettlement Activity of the Dogfish (Scyliorhinus Canicula) Eggcase , 1996, Journal of the Marine Biological Association of the United Kingdom.

[84]  C. Amsler,et al.  Individual and Coupled Effects of Echinoderm Extracts and Surface Hydrophobicity on Spore Settlement and Germination in the Brown Alga Hincksia irregularis , 2003, Biofouling.

[85]  W. Barthlott,et al.  Purity of the sacred lotus, or escape from contamination in biological surfaces , 1997, Planta.

[86]  P. Steinberg,et al.  ULTRASTRUCTURE OF THE GLAND CELLS OF THE RED ALGA ASPARAGOPSIS ARMATA (BONNEMAISONIACEAE) 1 , 2006 .

[87]  Philip Ball,et al.  Engineering Shark skin and other solutions , 1999, Nature.

[88]  M. Pereira,et al.  10 – Legislation affecting antifouling products , 2009 .

[89]  T. Hodgkiess,et al.  A Replica Method for the Study of Marine Biofilms , 1995, Journal of the Marine Biological Association of the United Kingdom.

[90]  R. Nys,et al.  Chemical antifouling defences of sea stars: effects of the natural products hexadecanoic acid, cholesterol, lathosterol and sitosterol , 2009 .

[91]  R. Nys,et al.  A new method for determining surface concentrations of marine natural products on seaweeds , 1998 .

[92]  Jian Ji,et al.  Interaction of Zoospores of the Green Alga Ulva with Bioinspired Micro‐ and Nanostructured Surfaces Prepared by Polyelectrolyte Layer‐by‐Layer Self‐Assembly , 2010 .

[93]  P. Gatenholm,et al.  Design and microstructuring of PDMS surfaces for improved marine biofouling resistance , 2000, Journal of biomaterials science. Polymer edition.

[94]  Berntsson,et al.  Analysis of behavioural rejection of micro-textured surfaces and implications for recruitment by the barnacle Balanus improvisus. , 2000, Journal of experimental marine biology and ecology.

[95]  Adam W Feinberg,et al.  Engineered antifouling microtopographies – correlating wettability with cell attachment , 2006, Biofouling.

[96]  S. Mclean,et al.  Novel pseudopteranoids of , 1991 .

[97]  A. S. Braverman,et al.  Progress in Molecular and Subcellular Biology 3 , 1973, Progress in Molecular and Subcellular Biology.

[98]  Christopher J. Long,et al.  Engineered nanoforce gradients for inhibition of settlement (attachment) of swimming algal spores. , 2008, Langmuir : the ACS journal of surfaces and colloids.