Hostname: page-component-76fb5796d-45l2p Total loading time: 0 Render date: 2024-04-26T21:39:30.130Z Has data issue: false hasContentIssue false
  • English
  • Français

Parallel plications may enhance surface function: physical properties of transparent tunics in colonial ascidians Clavelina cyclus and C. obesa

Published online by Cambridge University Press:  15 October 2019

Daisuke Sakai ,
Hiroshi Kakiuchida ,
Kenji Harada ,
Jun Nishikawa Open the ORCID record for Jun Nishikawa [Opens in a new window]  and
Euichi Hirose Open the ORCID record for Euichi Hirose [Opens in a new window]
Daisuke Sakai
Affiliation:
School of Regional Innovation and Social Design Engineering, Kitami Institute of Technology, Koen-cho, Kitami, Hokkaido 090-8507, Japan
Hiroshi Kakiuchida
Affiliation:
Structural Materials Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Moriyama, Nagoya, Aichi 463-8560, Japan
Kenji Harada
Affiliation:
School of Regional Innovation and Social Design Engineering, Kitami Institute of Technology, Koen-cho, Kitami, Hokkaido 090-8507, Japan
Jun Nishikawa
Affiliation:
Department of Marine Biology, School of Marine Science and Technology, Tokai University, Orido, Shimizu, Shizuoka 424-8610, Japan
Euichi Hirose*
Affiliation:
Faculty of Science, University of the Ryukyus, Nishihara, Okinawa 903-0213, Japan
*
Author for correspondence: Euichi Hirose, E-mail: euichi@sci.u-ryukyu.ac.jp
Get access Rights & Permissions [Opens in a new window]

Abstract

An array of nano-scale protrusions, called the nipple array, is found on the body surface of various invertebrates, and this structure is believed to decrease light reflectance and water wettability on the surface in the terrestrial environment. However, its potential functions have not been well studied in aquatic environments. Clavelina spp. are colonial ascidians that have the nipple array on their integumentary matrix (i.e. tunic). We examined the physical properties on the surface of the tunic of C. cyclus and C. obesa, such as hardness, wettability and refractive indices, to evaluate the functional importance of this structure. The tunic cuticle of both species was covered with the nipple array, and the cuticle of C. cyclus was bent into folds forming parallel plications. The Clavelina tunic was very soft and had high bubble- and oil-repellency. The refractive-index deviation between the tunic and seawater was 0.07–0.095 for 589-nm light (D-line). Rigorous coupled wave analysis (RCWA) showed that the nipple array slightly reduced reflectance on the surface and the parallel plications reduced the reflectance still more. The nanoimprinted plates imitating the parallel plications have higher bubble repellency and lower reflectance than the flat plates. These findings support the functional importance of the plications as well as the nipple array.

Keywords

Hardnesslight reflectionnanoimprintingnipple arrayrigorous coupled wave analysisspectroscopic ellipsometryultrastructurewettability
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 8 , December 2019 , pp. 1831 - 1839
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Authors contributed equally to this study.

References

Ballarin, L, Franchi, N, Gasparini, F, Caicci, F, Miyauchi, A and Hirose, E (2015) Suppression of cell-spreading and phagocytic activity on nano-pillared surface: in vitro experiment using hemocytes of the colonial ascidian Botryllus schlosseri. Invertebrate Survival Journal 12, 82–88.Google Scholar
Belton, PS, Tanner, SF, Cartier, N and Chanzy, H (1989) High-resolution solid-state 13C nuclear magnetic resonance spectroscopy of tunicin, an animal cellulose. Macromolecules 22, 1615–1617.Google Scholar
Bernhard, CG (1967) Structural and functional adaptation in a visual system. Endeavour 26, 79–84.Google Scholar
Cloney, RA (1994) Test cell secretions and their functions in ascidian development. In Wilson, W, Stricker, S and Shinn, G (eds), Reproduction and Development of Marine Invertebrates. Baltimore, MD: Johns Hopkins University Press, pp. 77–95.Google Scholar
Hirai, Y, Yabu, Y, Kaido, M, Suzuki, A and Shimomura, M (2013) Ag micro-dimples prepared by self-organization and their friction properties. Kobunshi Ronbunshu 70, 193–198. (In Japanese with English abstract.)Google Scholar
Hirose, E and Sensui, N (2019) Does nano-scale nipple array (moth-eye structure) suppress the settlement of ascidian larvae? Journal of the Marine Biological Association of the United Kingdom 99, 1393–1397.Google Scholar
Hirose, E and Uyeno, D (2014) Histopathology of a mesoparasitic hatschekiid copepod in hospite: does Mihbaicola sakamakii (Copepoda: Siphonostomatoida: Hatschekiidae) fast within the host fish tissue? Zoological Science 31, 546–552.Google Scholar
Hirose, E, Saito, Y, Hashimoto, K and Watanabe, H (1990) Minute protrusions of the cuticle – fine surface structures of the tunic in ascidians. Journal of Morphology 204, 67–73.Google Scholar
Hirose, E, Nishikawa, T, Saito, Y and Watanabe, H (1992) Minute protrusions of ascidian tunic cuticle – some implications for ascidian phylogeny. Zoological Science 9, 405–412.Google Scholar
Hirose, E, Lambert, G, Kusakabe, T and Nishikawa, T (1997) Tunic cuticular protrusions in ascidians (Chordata, Tunicata): a perspective of their character-state distribution. Zoological Science 14, 683–689.Google Scholar
Hirose, E, Kimura, S, Itoh, T and Nishikawa, J (1999) Tunic morphology and cellulosic components of pyrosomas, doliolids, and salps (Thaliacea, Urochordata). The Biological Bulletin 196, 113–120.Google Scholar
Hirose, E, Mayama, H and Miyauchi, A (2013) Does the aquatic invertebrate nipple array prevent bubble adhesion? An experiment using nanopillar sheets. Biology Letters 9, 20130552.Google Scholar
Hirose, E, Sakai, D, Shibata, T, Nishii, J, Mayama, H, Miyauchi, A and Nishikawa, J (2015) Does the tunic nipple array serve to camouflage diurnal salps? Journal of the Marine Biological Association of the United Kingdom 95, 1025–1031.Google Scholar
Hirose, E, Nakayama, K, Yanagida, T, Nawata, A and Kitamura, S-I (2018) Measurement of tunic hardness in an edible ascidian, Halocynthia roretzi, with remarks on soft tunic syndrome. Zoological Science 35, 548–552.Google Scholar
Inoue, J, Nakashima, K and Satoh, N. (2019) ORTHOSCOPE analysis reveals the presence of the cellulose synthase gene in all tunicate genomes but not in other animal genomes. Genes 10, 294.Google Scholar
Iseto, T and Hirose, E (2010) Comparative morphology of the foot structure of four genera of Loxosomatidae (Entoprocta): implications for foot functions and taxonomy. Journal of Morphology 271, 1185–1196.Google Scholar
Ivanova, EP, Hasan, J, Webb, HK, Truong, VK, Watson, GS, Watson, JA, Baulin, VA, Pogodin, S, Wang, JY, Tobin, MJ, Löbbe, C and Crawford, RJ (2012) Natural bactericidal surfaces: mechanical rupture of Pseudomonas aeruginosa cells by cicada wings. Small 8, 2489–2494.Google Scholar
Ivanova, EP, Hasan, J, Webb, HK, Gervinskas, G, Juodkazis, S, Truong, VK, Wu, AHF, Lamb, RN, Baulin, VA, Watson, GS, Watson, JA, Mainwaring, DE and Crawford, RJ (2013) Bactericidal activity of black silicon. Nature Communications 4, 1–7.Google Scholar
Kakiuchida, H, Sakai, D, Nishikawa, J and Hirose, E (2017) Measurement of refractive indices of tunicates' tunic: light reflection of the transparent integuments in an ascidian Rhopalaea sp. and a salp Thetys vagina. Zoological Letters 3, 7.Google Scholar
Kimura, S, Ohshima, C, Hirose, E, Nishikawa, J and Itoh, T. (2001) Cellulose in the house of the appendicularian Oikopleura rufescens. Protoplasma 216, 71–74.Google Scholar
Nomura, S, Kojima, H, Ohyabu, Y, Kuwabara, K, Miyauchi, A and Uemura, T (2005) Cell culture on nanopillar sheet: study of HeLa cells on nanopillar sheet. Japanese Journal of Applied Physics 44, 1184–1186.Google Scholar
Parker, A (2003) In the Blink of an Eye. Cambridge, MA: Perseus Publishing.Google Scholar
Peisker, H and Gorb, SN (2010) Always on the bright side of life: anti-adhesive properties of insect ommatidia grating. Journal of Experimental Biology 213, 3457–3462.Google Scholar
Quan, X and Fry, ES (1995) Empirical equation for the index of refraction of seawater. Applied Optics 34, 3477–3480.Google Scholar
R Core Team (2018) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/.Google Scholar
Sakai, D, Kakiuchida, H, Nishikawa, J and Hirose, E (2018) Physical properties of the tunic in the pinkish-brown salp Pegea confoederata (Tunicata: Thaliacea). Zoological Letters 4, 7.Google Scholar
Van Daele, Y, Revol, J, Gaill, F and Goffinet, G (1992) Characterization and supramolecular architecture of the cellulose-protein fibrils in the tunic of the sea peach (Halocynthia papillosa, Ascidiacea, Urochordata). Biology of the Cell 76, 86–97.Google Scholar
Wilson, SJ and Hutley, MC (1982) The optical properties of “moth eye” antireflection surfaces. Optica Acta 29, 993–1009.Google Scholar
Supplementary material: Image

Sakai et al. supplementary material

Sakai et al. supplementary material 1

Download Sakai et al. supplementary material(Image)
Image 524.5 KB
Supplementary material: Image

Sakai et al. supplementary material

Sakai et al. supplementary material 2

Download Sakai et al. supplementary material(Image)
Image 2.6 MB