Skip to main content

Progress in the Study of Adhesion by Marine Invertebrate Larvae

  • Chapter
  • First Online:
Biological Adhesives

Abstract

This chapter summarises recent progress towards the characterisation of bioadhesives secreted by the larvae of marine invertebrates, with reference also to their subsequent developmental stages. These adhesives vary structurally and biochemically between species and between life stages to satisfy the requirements of the particular organism for permanent or temporary/reversible adhesion, often under hostile conditions. To date, a small number of bioadhesives have been described for the adult forms of marine invertebrates, while a functional understanding of larval adhesives remains elusive. Progress is essential, however, since the larval forms perform a key role in the fouling of marine structures, and their adhesives may have characteristics of interest for development of synthetic, bio-inspired glues. Despite recent advances in the fields of proteomics and genomics, major obstacles exist in the isolation and analysis of tiny quantities of larval adhesives, which have largely precluded these approaches. Further challenges relate to the in situ detection of larval adhesive materials, being usually secreted underwater and buried at the interface between a solid substrate and the organism’s body. Here, we discuss a range of novel experimental approaches that have surmounted these technical issues and provided useful insight into the morphology and composition of larval bioadhesives in situ. These involve imaging and spectroscopic approaches as well as nano-/micromechanical and surface-sensitive techniques that have enabled quantification of adhesion forces and surface adsorption of purified adhesive proteins.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aldred N, Clare AS (2008) The adhesive strategies of cyprids and development of barnacle-resistant marine coatings. Biofouling 24:351–363

    Article  CAS  PubMed  Google Scholar 

  • Aldred N, Clare AS (2014) Mini-review: impact and dynamics of surface fouling by solitary and compound ascidians. Biofouling 30:259–270

    Article  PubMed  Google Scholar 

  • Aldred N, Ista LK, Callow ME et al (2006) Mussel (Mytilus edulis) byssus deposition in response to variations in surface wettability. J R Soc Interface 3:37–43

    Article  CAS  PubMed  Google Scholar 

  • Aldred N, Ekblad T, Andersson O et al (2011) Real-time quantification of microscale bioadhesion events in situ using imaging surface plasmon resonance (iSPR). Appl Mater Interfaces 3:2085–2091

    Article  CAS  Google Scholar 

  • Aldred N, Høeg JT, Maruzzo D et al (2013a) Analysis of the behaviours mediating barnacle cyprid reversible adhesion. PLoS One 8:e68085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aldred N, Gohad NV, Petrone L et al (2013b) Confocal microscopy-based goniometry of barnacle cyprid permanent adhesive. J Exp Biol 216:1969–1972

    Article  PubMed  Google Scholar 

  • Andersson O, Ekblad T, Aldred N et al (2009) Novel application of imaging surface plasmon resonance for in situ studies of the surface exploration of marine organisms. Biointerphases 4:65–68

    Article  CAS  PubMed  Google Scholar 

  • Barlow DE, Wahl KJ (2012) Optical spectroscopy of marine bioadhesives interfaces. Annu Rev Anal Chem 5:229–251

    Article  CAS  Google Scholar 

  • Barlow DE, Dickinson GH, Orihuela B et al (2009) In situ characterization of the primary cement interfaces of the barnacle Balanus amphitrite. Biofouling 25:359–366

    Article  CAS  PubMed  Google Scholar 

  • Barlow DE, Dickinson GH, Orihuela B et al (2010) Characterization of the adhesive plaque of the barnacle Balanus amphitrite: Amyloid-like nanofibrils are a major component. Langmuir 26:6549–6556

    Article  CAS  PubMed  Google Scholar 

  • Berglin M, Hedlund J, Fant C et al (2005) Use of surface-sensitive methods for the study of adsorption and cross-linking of marine bioadhesives. J Adhes 81:805–822

    Article  CAS  Google Scholar 

  • Burden DK, Barlow DE, Spillmann CM et al (2012) Barnacle Balanus amphitrite adheres by a stepwise cementing process. Langmuir 28:13364–13372

    Article  CAS  PubMed  Google Scholar 

  • Burkett JR, Hight LM, Kenny P et al (2010) Oysters produce an organic–inorganic adhesive for intertidal reef construction. J Am Chem Soc 132:12531–12533

    Article  CAS  PubMed  Google Scholar 

  • Callaway E (2015) The revolution will not be crystallized: A new method sweeps through structural biology. Nature 525:172–174

    Article  CAS  PubMed  Google Scholar 

  • Callow JA, Crawford SA, Higgins MJ et al (2000) The application of atomic force microscopy to topographical studies and force measurements on the secreted adhesive of the green alga Enteromorpha. Planta 211:641–647

    Article  CAS  PubMed  Google Scholar 

  • Callow JA, Osborne MP, Callow ME et al (2003) Use of environmental scanning electron microscopy to image the spore adhesive of the marine alga Enteromorpha in its natural hydrated state. Colloid Surf B 27:315–321

    Article  CAS  Google Scholar 

  • Callow JA, Callow ME, Ista LK et al (2005) The influence of surface energy on the wetting behaviour of the spore adhesive of the marine alga Ulva linza (synonym Enteromorpha linza). J R Soc Interface 2:319–325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiovitti A, Dugdale TM, Wetherbee R (2006) Diatom adhesives: molecular and mechanical properties. In: Smith AM, Callow JA (eds) Biological adhesives. Springer, Heidelberg, pp 79–103

    Chapter  Google Scholar 

  • Clare AS, Aldred N (2009) Surface colonisation by marine organisms and its impact on antifouling research. In: Hellio C, Yebra D (eds) Advances in marine antifouling coatings and technologies. Woodhead Publishing, Oxford, pp 46–79

    Chapter  Google Scholar 

  • Connor PA, Dobson KD, McQuillan AJ (1995) New sol–gel attenuated total reflection infrared spectroscopic method for analysis of adsorption at metal oxide surfaces in aqueous solutions. chelation of TiO2, ZrO2 and Al2O3 surfaces by catechol, 8-quinolinol, and acetylacetone. Langmuir 11:4193–4195

    Article  CAS  Google Scholar 

  • Crisp DJ (1976) Two settlement responses in marine organisms. In: Newell RC (ed) Adaptation to environment. Essays on the physiology of marine animals. Butterworths, London, pp 83–124

    Chapter  Google Scholar 

  • Dahms HU, Dobretsov S, Qian PY (2004) The effect of bacterial and diatom biofilms on the settlement of the bryozoan Bugula neritina. J Exp Mar Biol Ecol 313:191–209

    Article  Google Scholar 

  • Dreanno C, Matsumura K, Dohmae N (2006a) An α2-macroglobulin-like protein is the cue to gregarious settlement of the barnacle. Proc Natl Acad Sci USA 103:14396–14401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dreanno C, Kirby RR, Clare AS (2006b) Smelly feet are not always a bad thing: The relationship between cyprid footprint protein and the barnacle settlement pheromone. Biol Lett 2:423–425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dugdale TM, Dagastine R, Chiovitti A (2005) Single adhesive nanofibres from a live diatom have the signature fingerprint of modular proteins. Biophys J 89:4252–4260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dugdale TM, Dagastine R, Chiovitti A et al (2006a) Diatom adhesive mucilage contains distinct supramolecular assemblies of a single modular protein. Biophys J 90:2987–2993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dugdale TM, Willis A, Wetherbee R (2006b) Adhesive modular proteins occur in the extracellular mucilage of the motile, pennate diatom Phaeodactylum tricornutum. Biophys J 90:L58–L60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Federle W, Riehle M, Curtis ASG et al (2002) An integrative study of insect adhesion: mechanics and wet adhesion of pretarsal pads in ants. Integr Comp Biol 42:1100–1106

    Article  PubMed  Google Scholar 

  • Gao Z, Bremer PJ, Barker MF et al (2007) Adhesive secretions of live mussels observed in situ by attenuated total reflection-infrared spectroscopy. Appl Spectrosc 61:55–9

    Article  CAS  PubMed  Google Scholar 

  • Gohad NV, Aldred N, Orihuela B et al (2012) Observations on the settlement and cementation of the barnacle (Balanus amphitrite) cyprid larvae after artificial exposure to noradrenaline and the locations of adrenergic-like receptors. J Exp Mar Biol Ecol 416–417:153–161

    Article  Google Scholar 

  • Gohad NV, Aldred N, Hartshorn CM et al (2014) Synergistic roles for lipids and proteins in the permanent adhesive of barnacle larvae. Nat Commun 5:4414

    Article  CAS  PubMed  Google Scholar 

  • Golden JP, Burden DK, Fears KP et al (2016) Imaging active surface processes in barnacle adhesive interfaces. Langmuir 32(2):541–550. doi:10.1021/acs.langmuir.5b03286

    Article  CAS  PubMed  Google Scholar 

  • Goormaghtigh E, Raussens V, Ruysschaert J-M (1999) Attenuated total reflection infrared spectroscopy of proteins and lipids in biological membranes. Biochim Biophys A 1422:105–185

    Article  CAS  Google Scholar 

  • Grosser K, Zedler L, Schmitt M et al (2012) Disruption-free imaging by Raman spectroscopy reveals a chemical sphere with antifouling metabolites around macroalgae. Biofouling 28:687–696

    Article  CAS  PubMed  Google Scholar 

  • Haesaerts D, Jangoux M, Flammang P (2005) The attachment complex of brachiolaria larvae of the sea star Asterias rubens (Echinodermata): an ultrastructural and immunocytochemical study. Zoomorphology 124:67–78

    Article  Google Scholar 

  • Harrington MJ, Masic A, Holten-Andersen N et al (2010) Iron-clad fibers: a metal-based biological strategy for hard flexible coatings. Science 328:216–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He L-S, Zhang G, Qian P-Y (2013) Characterization of two 20kDa-cement protein (cp20k) homologues in Amphibalanus amphitrite. PLoS One 8(5), e64130

    Article  PubMed  PubMed Central  Google Scholar 

  • Hennebert E, Maldonado B, Van De Weerdt C et al (2015) From sand tube to test tube: the adhesive secretion from Sabellariid tubeworms. In: Bianco-Peled H, Davidovich-Pinhas M (eds) Bioadhesion and biomimetics: from nature to applications. CRC Press, Boca Raton, pp 109–127

    Google Scholar 

  • Higgings MJ, Molino P, Mulvaney P et al (2003) The structure and nanomechanical properties of the adhesive mucilage that mediates diatom substratum adhesion and motility. J Phycol 39:1181–1193

    Article  Google Scholar 

  • Higgins MJ, Crawford SA, Mulvaney P et al (2000) The topography of soft, adhesive diatom ‘trails’ as observed by atomic force microscopy. Biofouling 16:133–139

    Article  Google Scholar 

  • Higgins MJ, Crawford SA, Mulvaney P et al (2002) Characterization of the adhesive mucilage secreted by live diatom cells using atomic force microscopy. Protist 153:25–38

    Article  PubMed  Google Scholar 

  • HÓ§Ó§k F, Kasemo B, Nylander T et al (2001) Variations in coupled water, viscoelastic properties, and film thickness of a Mefp1 protein film during adsorption and cross-linking: a quartz crystal microbalance with dissipation monitoring, ellipsometry, and surface plasmon resonance study. Anal Chem 73:5796–5804

    Article  Google Scholar 

  • Hug SJ (1997) In situ Fourier transform infrared measurements of sulfate adsorption on hematite in aqueous solutions. J Colloid Interface Sci 188:415–422

    Article  CAS  Google Scholar 

  • Hug SJ, Sulzberger B (1994) In situ Fourier transform infrared spectroscopic evidence for the formation of several different surface complexes of oxalate on TiO2 in the aqueous phase. Langmuir 10:3587–3597

    Article  CAS  Google Scholar 

  • Kamino K (2013) Mini-review: Barnacle adhesives and adhesion. Biofouling 29:735–749

    Article  CAS  PubMed  Google Scholar 

  • Lee BP, Messersmith BP, Israelachvili JN et al (2011) Mussel-inspired adhesives and coatings. Annu Rev Mater Res 41:99–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maleshlijski S, Sendra GH, Di Fino A et al (2012) Three dimensional tracking of exploratory behaviour of barnacle cyprids using stereoscopy. Biointerphases 7:50

    Google Scholar 

  • Maleshlijski S, Sendra GH, Aldred N et al (2015) Imaging SPR combined with stereoscopic 3D tracking to study barnacle cyprid-surface interactions. Surf Sci 643:172–177

    Article  Google Scholar 

  • Martinez Rodriguez NR, Das S, Kaufman Y et al (2015) Interfacial pH during mussel adhesive plaque formation. Biofouling 31:221–227

    Article  CAS  PubMed  Google Scholar 

  • McQuillan AJ (2001) Probing solid-solution interfacial chemistry with ATR-IR spectroscopy of particle films. Adv Mater 13:1034–1038

    Article  CAS  Google Scholar 

  • McWhirter MJ, Bremer PJ, Lamont IL et al (2003) Siderophore-mediated covalent bonding to metal (oxide) surfaces during biofilm initiation by Pseudomonas aeruginosa bacteria. Langmuir 19:3575–3577

    Article  CAS  Google Scholar 

  • Mostaert AS, Giordani C, Crockett R et al (2009) Characterisation of amyloid nanostructures in the natural adhesive of unicellular subaerial algae. J Adhes 85:465–483

    Article  CAS  Google Scholar 

  • Nakano M, Kamino K (2015) Amyloid-like conformation and the interaction for the self-assembly in barnacle underwater cement. Biochemistry 54:826–835

    Article  CAS  PubMed  Google Scholar 

  • Nott JA, Foster BA (1969) On the structure of the antennular attachment organ of the cypris larva of Balanus balanoides (L.). Philos Trans R Soc B 256:115–134

    Article  Google Scholar 

  • Parikh SJ, Chorover J (2006) ATR-FTIR spectroscopy reveals bond formation during bacterial adhesion to iron oxide. Langmuir 22:8492–500

    Article  CAS  PubMed  Google Scholar 

  • Peak D, Ford RG, Sparks DL (1999) An in Situ ATR-FTIR investigation of sulfate bonding mechanisms on goethite. J Colloid Interface Sci 218:289–299

    Article  CAS  PubMed  Google Scholar 

  • Petrone L (2013) Molecular surface chemistry in marine bioadhesion. Adv Colloid Interface Sci 195–196:1–18

    Article  PubMed  Google Scholar 

  • Petrone L, McQuillan AJ (2011) Alginate ion adsorption on a TiO2 particle film and interactions of adsorbed alginate with calcium ions investigated by Attenuated Total Reflection Infrared (ATR-IR) spectroscopy. Appl Spectrosc 65:1162–1169

    Article  PubMed  Google Scholar 

  • Petrone L, Ragg NLC, McQuillan AJ (2008) In situ infrared spectroscopic investigation of Perna canaliculus mussel larvae primary settlement. Biofouling 24:405–413

    Article  CAS  PubMed  Google Scholar 

  • Petrone L, Ragg NLC, Girvan L (2009) Scanning electron microscopy and energy dispersive X-ray microanalysis of Perna canaliculus mussel larvae adhesive secretion. J Adhes 85:78–96

    Article  CAS  Google Scholar 

  • Petrone L, Easingwood R, Barker MF et al (2011a) In situ ATR-IR spectroscopic and electron microscopic analyses of settlement secretions of Undaria pinnatifida kelp spores. J R Soc Interface 8:410–422

    Article  CAS  PubMed  Google Scholar 

  • Petrone L, DiFino A, Aldred N et al (2011b) Effects of surface charge and Gibbs surface energy on the settlement behaviour of barnacle cyprids (Balanus amphitrite). Biofouling 27:1043–1055

    Article  PubMed  Google Scholar 

  • Petrone L, Kumar A, Sutanto CN et al (2015a) Mussel adhesion is dictated by time-regulated secretion and molecular conformation of mussel adhesive proteins. Nat Commun 6:8737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petrone L, Aldred N, Emami K et al (2015b) Chemistry-specific surface adsorption of the barnacle settlement-inducing protein complex. Interface Focus 5:20140047

    Article  PubMed  PubMed Central  Google Scholar 

  • Phang IY, Aldred N, Clare AS et al (2006) An in situ study of the nanomechanical properties of barnacle (Balanus amphitrite) cyprid cement using atomic force microscopy (AFM). Biofouling 22:245–250

    Article  PubMed  Google Scholar 

  • Phang IY, Aldred N, Clare AS et al (2008) Towards a nanomechanical basis for temporary adhesion in barnacle cyprids (Semibalanus balanoides). J R Soc Interface 5:397–402

    Article  CAS  PubMed  Google Scholar 

  • Phang IY, Aldred N, Ling XY et al (2010) Atomic force microscopy of the morphology and mechanical behaviour of barnacle cyprid footprint proteins at the nanoscale. J R Soc Interface 7:285–296

    Article  CAS  PubMed  Google Scholar 

  • Schmidt M, Cavaco A, Gierlinger N et al (2009) In situ imaging of barnacle (Balanus amphitrite) cyprid cement using confocal Raman microscopy. J Adhes 85:139–151

    Article  CAS  Google Scholar 

  • Senkbeil T, Mohamed T, Simon R et al (2016) In vivo and in situ synchrotron radiation μ-XRF reveals elemental distributions during the early attachment phase of barnacle larvae and juvenile barnacles. Anal Bioanal Chem 408(5):1487–1496

    Article  CAS  PubMed  Google Scholar 

  • Sperline RP, Song Y, Freiser H (1992) Fourier transform infrared attenuated total reflection spectroscopy linear dichroism study of sodium dodecyl sulfate adsorption at the alumina/water interface using alumina-coated optics. Langmuir 8:2183–2191

    Article  CAS  Google Scholar 

  • Strathmann R (1978) Length of pelagic period in echinoderms with feeding larvae from the Northeast Pacific. J Exp Mar Biol Ecol 34:23–27

    Article  Google Scholar 

  • Tanur AE, Gunari NA, Sullan RM et al (2009) Biomineralisation by the marine tubeworm Hydroides dianthus and composition of the adhesive cement. Biophys J 96:640–641

    Article  Google Scholar 

  • Walker G (1971) A study of the cement apparatus of the cypris larva of the barnacle Balanus balanoides. Mar Biol 9:205–212

    Article  Google Scholar 

  • Walker G, Yule AB (1984a) Temporary adhesion of the barnacle cyprid: The existence of an antennular adhesive secretion. J Mar Biol Assoc UK 64:679–686

    Article  Google Scholar 

  • Walker G, Yule AB (1984b) The temporary adhesion of barnacle cyprids: effects of some differing surface characteristics. J Mar Biol Assoc UK 1984(64):429–439

    Google Scholar 

  • Wei W, Tan Y, Martinez Rodriguez NR et al (2014) A mussel-derived one component adhesive coacervate. Acta Biomater 10:1663–1670

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Wei W, Danner E et al (2011) Effects of interfacial redox in mussel adhesive protein films on mica. Proc Natl Acad Sci USA 23:2362–2366

    CAS  Google Scholar 

Download references

Acknowledgements

N. Aldred acknowledges funding support from the Office of Naval Research award number N00014-13-1-0634 to A. S. Clare and N. Aldred. N. Aldred receives additional support from a Newcastle University SAgE Faculty Research Fellowship. Both authors would like to extend their gratitude to Prof. A. M. Smith for the invitation to contribute a chapter to this edited volume.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nick Aldred .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Aldred, N., Petrone, L. (2016). Progress in the Study of Adhesion by Marine Invertebrate Larvae. In: Smith, A. (eds) Biological Adhesives. Springer, Cham. https://doi.org/10.1007/978-3-319-46082-6_4

Download citation

Publish with us

Policies and ethics