Wing wettability gradient in a damselfly Lestes sponsa (Odonata: Lestidae) reflects the submergence behaviour during underwater oviposition
Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
33489275
PubMed Central
PMC7813233
DOI
10.1098/rsos.201258
PII: rsos201258
Knihovny.cz E-zdroje
- Klíčová slova
- Odonata, hydrophobicity, insect wings, nanostructures, submerged oviposition, wettability,
- Publikační typ
- časopisecké články MeSH
The phenomenon of hydrophobicity of insect cuticles has received great attention from technical fields due to its wide applicability to industry or medicine. However, in an ecological/evolutionary context such studies remain scarce. We measured spatial differences in wing wettability in Lestes sponsa (Odonata: Lestidae), a damselfly species that can submerge during oviposition, and discussed the possible functional significance. Using dynamic contact angle (CA) measurements together with scanning electron microscopy (SEM), we investigated differences in wettability among distal, middle and proximal wing regions, and in surface nanostructures potentially responsible for observed differences. As we moved from distal towards more proximal parts, mean values of advancing and receding CAs gradually increased from 104° to 149°, and from 67° to 123°, respectively, indicating that wing tips were significantly less hydrophobic than more proximal parts. Moreover, values of CA hysteresis for the respective wing parts decreased from 38° to 26°, suggesting greater instability of the structure of the wing tips. Accordingly, compared with more proximal parts, SEM revealed higher damage of the wax nanostructures at the distal region. The observed wettability gradient is well explained by the submergence behaviour of L. sponsa during underwater oviposition. Our study thus proposed the existence of species-dependent hydrophobicity gradient on odonate wings caused by different ovipositional strategies.
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Byun D, Hong J, Saputra KJ, Lee YJ, Park HC, Byun B-K, Lukes JR. 2009. Wetting characteristics of insect wing surfaces. J. Bionic Eng. 6, 63–70. (10.1016/S1672-6529(08)60092-X) DOI
Watson GS, Cribb BW, Watson JA. 2011. Contrasting micro/nano architecture on termite wings: two divergent strategies for optimising success of colonisation flights. PLoS ONE 6, e24368 (10.1371/journal.pone.0024368) PubMed DOI PMC
Wagner T, Neinhuis C, Barthlott W. 1996. Wettability and contaminability of insect wings as a function of their surface sculptures. Acta Zool. 77, 213–225. (10.1111/j.1463-6395.1996.tb01265.x) DOI
Sun M, Watson GS, Zheng Y, Watson JA, Liang A. 2009. Wetting properties on nanostructured surfaces of cicada wings. J. Exp. Biol. 212, 3148–3155. (10.1242/jeb.033373) PubMed DOI
Kesel AB, Philippi U, Nachtigall W. 1998. Biomechanical aspects of the insect wing: an analysis using the finite element method. Comput. Biol. Med. 28, 423–437. (10.1016/S0010-4825(98)00018-3) PubMed DOI
Holdgate MW. 1955. The wetting of insect cuticles by water. J. Exp. Biol. 32, 591–617.
Nguyen SHT, Webb HK, Hasan J, Tobin MJ, Crawford RJ, Ivanova EP. 2013. Dual role of outer epicuticular lipids in determining the wettability of dragonfly wings. Colloids Surf. B Biointerfaces 106, 126–134. (10.1016/j.colsurfb.2013.01.042) PubMed DOI
Webb HK, Crawford RJ, Ivanova EP. 2014. Wettability of natural superhydrophobic surfaces. Adv. Colloid Interface Sci. 210, 58–64. (10.1016/j.cis.2014.01.020) PubMed DOI
Gorb SN, Kesel A, Berger J. 2000. Microsculpture of the wing surface in Odonata: evidence for cuticular wax covering. Arthropod Struct. Dev. 29, 129–135. (10.1016/S1467-8039(00)00020-7) PubMed DOI
Hirayama H, Kasuya E. 2008. Factors affecting submerged oviposition in a water strider: level of dissolved oxygen and male presence. Anim. Behav. 76, 1919–1926. (10.1016/j.anbehav.2008.08.013) DOI
Watson GS, Cribb BW, Watson JA. 2010. How micro/nanoarchitectures facilitates anti-wetting: an elegant hierarchical design on the termite wing. ACS Nano 4, 129–136. (10.1021/nn900869b) PubMed DOI
Sun M, Liang A, Watson GS, Watson JA, Zheng Y, Ju J, Jiang L. 2012. Influence of cuticle nanostructuring on the wetting behaviour/states on cicada wings. PLoS ONE 7, e35056 (10.1371/journal.pone.0035056) PubMed DOI PMC
Tobin MJ, et al. 2015. Fourier transform infrared spectroscopy and imaging of dragonfly, damselfly and cicada wing membranes. Spectrosc. Eur. 27, 15.
Oh J, et al. 2017. Exploring the role of habitat on the wettability of cicada wings. ACS Appl. Mater. Interfaces 9, 27 173–27 184. (10.1021/acsami.7b07060) PubMed DOI
Sun J, Bhushan B. 2012. The structure and mechanical properties of dragonfly wings and their role on flyability. Comptes Rendus Mécanique 340, 3–17. (10.1016/j.crme.2011.11.003) DOI
Ivanova EP, et al. 2013. Molecular organization of the nanoscale surface structures of the dragonfly Hemianax papuensis wing epicuticle. PLoS ONE 8, e67893 (10.1371/journal.pone.0067893) PubMed DOI PMC
Darmanin T, Guittard F. 2015. Superhydrophobic and superoleophobic properties in nature. Mater. Today 18, 273–285. (10.1016/j.mattod.2015.01.001) DOI
Oh J, et al. 2019. Cicada-inspired self-cleaning superhydrophobic surfaces. J. Heat Transf. 141, 100905 (10.1115/1.4044677) DOI
Quéré D, Lafuma A, Bico J. 2003. Slippy and sticky microtextured solids. Nanotechnology 14, 1109–1112. (10.1088/0957-4484/14/10/307) DOI
Bhushan B, Jung YC, Koch K. 2009. Micro-, nano- and hierarchical structures for superhydrophobicity, self-cleaning and low adhesion. Phil. Trans. R. Soc. A 367, 1631–1672. (10.1098/rsta.2009.0014) PubMed DOI
Shirtcliffe NJ, McHale G, Atherton S, Newton MI. 2010. An introduction to superhydrophobicity. Adv. Colloid Interface Sci. 161, 124–138. (10.1016/j.cis.2009.11.001) PubMed DOI
Ivanova EP, et al. 2012. Natural bactericidal surfaces: mechanical rupture of Pseudomonas aeruginosa cells by cicada wings. Small 8, 2489–2494. (10.1002/smll.201200528) PubMed DOI
Bandara CD, Singh S, Afara IO, Wolff A, Tesfamichael T, Ostrikov K, Oloyede A. 2017. Bactericidal effects of natural nanotopography of dragonfly wing on Escherichia coli. ACS Appl. Mater. Interfaces 9, 6746–6760. (10.1021/acsami.6b13666) PubMed DOI
McHale G, Shirtcliffe NJ, Newton MI. 2004. Super-hydrophobic and super-wetting surfaces: analytical potential? Analyst 129, 284–287. (10.1039/b400567h) DOI
Marmur A. 2004. The Lotus effect: superhydrophobicity and metastability. Langmuir 20, 3517–3519. (10.1021/la036369u) PubMed DOI
Watson GS, Myhra S, Cribb BW, Watson JA. 2008. Putative functions and functional efficiency of ordered cuticular nanoarrays on insect wings. Biophys. J. 94, 3352–3360. (10.1529/biophysj.107.109348) PubMed DOI PMC
Watson GS, Cribb BW, Watson JA. 2010. The role of micro/nano channel structuring in repelling water on cuticle arrays of the lacewing. J. Struct. Biol. 171, 44–51. (10.1016/j.jsb.2010.03.008) PubMed DOI
Román-Kustas J, et al. 2020. Molecular and topographical organization: influence on cicada wing wettability and bactericidal properties. Adv. Mater. Interfaces 7, 2000112 (10.1002/admi.202000112) DOI
Hasan J, et al. 2012. Spatial variations and temporal metastability of the self-cleaning and superhydrophobic properties of damselfly wings. Langmuir 28, 17 404–17 409. (10.1021/la303560w) PubMed DOI
Nguyen SH, Webb HK, Hasan J, Tobin MJ, Mainwaring DE, Mahon PJ, Marchant R, Crawford RJ, Ivanova EP. 2014. Wing wettability of Odonata species as a function of quantity of epicuticular waxes. Vib. Spectrosc. 75, 173–177. (10.1016/j.vibspec.2014.07.006) DOI
Román-Kustas J, et al. 2020. Analysis of cicada wing surface constituents by comprehensive multidimensional gas chromatography for species differentiation. Microchem. J. 158, 105089 (10.1016/j.microc.2020.105089) DOI
Gorb SN, Tynkkynen K, Kotiaho JS. 2009. Crystalline wax coverage of the imaginal cuticle in Calopteryx splendens (Odonata: Calopterygidae). Int. J. Odonatol. 12, 205–221. (10.1080/13887890.2009.9748340) DOI
Tsubaki Y, Kato C, Shintani S. 2006. On the respiratory mechanism during underwater oviposition in a damselfly Calopteryx cornelia Selys. J. Insect Physiol. 52, 499–505. (10.1016/j.jinsphys.2006.01.009) PubMed DOI
Wan Y, Cong Q, Wang X, Yan Z. 2008. The wettability and mechanism of geometric non-smooth structure of dragonfly wing surface. J. Bionic Eng. 5, 40–45. (10.1016/S1672-6529(08)60070-0) DOI
Gao C-Y, Meng G-X, Li X, Wu M, Liu Y, Li X-Y, Zhao X, Lee I, Feng X. 2013. Wettability of dragonfly wings: the structure detection and theoretical modeling: wettability, modeling, and simulation of dragonfly wings. Surf. Interface Anal. 45, 650–655. (10.1002/sia.5105) DOI
Kuitunen K, Kovalev A, Gorb SN. 2014. Sex-related effects in the superhydrophobic properties of damselfly wings in young and old Calopteryx splendens. PLoS ONE 9, e88627 (10.1371/journal.pone.0088627) PubMed DOI PMC
Corbet PS. 1999. Dragonflies: behavior and ecology of Odonata. Colchester, UK: Harley Books.
Flynn MR, Bush JWM. 2008. Underwater breathing: the mechanics of plastron respiration. J. Fluid Mech. 608, 275–296. (10.1017/S0022112008002048) DOI
Aideo SN, Mohanta D. 2016. Limiting hydrophobic behavior and reflectance response of dragonfly and damselfly wings. Appl. Surf. Sci. 387, 609–616. (10.1016/j.apsusc.2016.06.049) DOI
Song F, Xiao KW, Bai K, Bai YL. 2007. Microstructure and nanomechanical properties of the wing membrane of dragonfly. Mater. Sci. Eng. A 457, 254–260. (10.1016/j.msea.2007.01.136) DOI
Nguyen S, Webb H, Mahon P, Crawford R, Ivanova E. 2014. Natural insect and plant micro-/nanostructsured surfaces: an excellent selection of valuable templates with superhydrophobic and self-cleaning properties. Molecules 19, 13 614–13 630. (10.3390/molecules190913614) PubMed DOI PMC
Kalkman VJ, et al. 2010. European red list of dragonflies. Luxembourg: Publications Office of the European Union.
Dolný A, Helebrandová J, Rusková T, Šigut M, Harabiš F. 2014. Ecological aspects of underwater oviposition in Lestes sponsa (Odonata: Lestidae). Odonatologica 43, 183–197.
Helebrandová J, Pyszko P, Dolný A. 2018. Large net cage for captive breeding and behavioural studies of damselfly Lestes sponsa (Hansemann, 1823) (Odonata: Lestidae): submerged oviposition as a model behaviour. Aquat. Insects 39, 43–53. (10.1080/01650424.2018.1432059) DOI
Stoks R, De Bruyn L, Matthysen E. 1997. The adaptiveness of intense contact mate guarding by males of the emerald damselfly, Lestes sponsa (Odonata, Lestidae): the male's perspective. J. Insect Behav. 10, 289–298. (10.1007/BF02765561) DOI
Johnson RE, Dettre RH. 1969. Wetting and contact angle. Surf. Colloid Sci. 2, 85–153.
Johnson RE, Dettre RH, Brandreth DA. 1977. Dynamic contact angles and contact angle hysteresis. J. Colloid Interface Sci. 62, 205–212. (10.1016/0021-9797(77)90114-X) DOI
Bhushan B, Jung YC. 2008. Wetting, adhesion and friction of superhydrophobic and hydrophilic leaves and fabricated micro/nanopatterned surfaces. J. Phys. Condens. Matter 20, 225010 (10.1088/0953-8984/20/22/225010) DOI
The MathWorks. 2015. MATLAB 2015a. Natick, MA: The MathWorks, Inc.
Outomuro D, Johansson F. 2019. Wing morphology and migration status, but not body size, habitat or Rapoport's rule predict range size in North-American dragonflies (Odonata: Libellulidae). Ecography 42, 309–320. (10.1111/ecog.03757) DOI
R Development Core Team. 2019. R: a language and environment for statistical computing. Vienna, Austria: The R Foundation for Statistical Computing; See https://www.r-project.org/.
Yan J. 2002. Geepack: yet another package for generalized estimating equations. R-News 2, 12–14.
Halekoh U, Højsgaard S, Yan J. 2006. The R package geepack for generalized estimating equations. J. Stat. Softw. 15, 1–11. (10.18637/jss.v015.i02) DOI
Lenth RV. 2016. Least-squares means: the R package lsmeans. J. Stat. Softw. 69, 1–33. (10.18637/jss.v069.i01) DOI
Koch K, Barthlott W. 2009. Superhydrophobic and superhydrophilic plant surfaces: an inspiration for biomimetic materials. Phil. Trans. R. Soc. A 367, 1487–1509. (10.1098/rsta.2009.0022) PubMed DOI
Webb HK, Hasan J, Truong VK, Crawford RJ, Ivanova EP. 2011. Nature inspired structured surfaces for biomedical applications. Curr. Med. Chem. 18, 3367–3375. (10.2174/092986711796504673) PubMed DOI
Su Y, Ji B, Zhang K, Gao H, Huang Y, Hwang K. 2010. Nano to micro structural hierarchy is crucial for stable superhydrophobic and water-repellent surfaces. Langmuir 26, 4984–4989. (10.1021/la9036452) PubMed DOI
Crawford R, Koopal LK, Ralston J. 1987. Contact angles on particles and plates. Colloids Surf. 27, 57–64. (10.1016/0166-6622(87)80133-6) DOI
Van Oss CJ, Good RJ, Chaudhury MK. 1988. Additive and nonadditive surface tension components and the interpretation of contact angles. Langmuir 4, 884–891. (10.1021/la00082a018) DOI
Lander LM, Siewierski LM, Brittain WJ, Vogler EA. 1993. A systematic comparison of contact angle methods. Langmuir 9, 2237–2239. (10.1021/la00032a055) DOI
Marmur A. 1994. Thermodynamic aspects of contact angle hysteresis. Adv. Colloid Interface Sci. 50, 121–141. (10.1016/0001-8686(94)80028-6) DOI
Gao L, McCarthy TJ. 2006. Contact angle hysteresis explained. Langmuir 22, 6234–6237. (10.1021/la060254j) PubMed DOI
Cheng Y-T, Rodak DE. 2005. Is the lotus leaf superhydrophobic? Appl. Phys. Lett. 86, 144101 (10.1063/1.1895487) DOI
Zhang J, Sheng X, Jiang L. 2009. The dewetting properties of lotus leaves. Langmuir 25, 1371–1376. (10.1021/la8024233) PubMed DOI
Bobji MS, Kumar SV, Asthana A, Govardhan RN. 2009. Underwater sustainability of the ‘Cassie’ state of wetting. Langmuir 25, 12 120–12 126. (10.1021/la902679c) PubMed DOI
Cassie ABD. 1948. Contact angles. Discuss. Faraday Soc. 3, 11–16. (10.1039/DF9480300011) DOI
Wenzel RN. 1949. Surface roughness and contact angle. J. Phys. Colloid Chem. 53, 1466–1467. (10.1021/j150474a015) DOI
Erbil HY, Cansoy CE. 2009. Range of applicability of the Wenzel and Cassie–Baxter equations for superhydrophobic surfaces. Langmuir 25, 14 135–14 145. (10.1021/la902098a) PubMed DOI
Patankar NA. 2004. Transition between superhydrophobic sates on rough surfaces. Langmuir 20, 7097–7102. (10.1021/la049329e) PubMed DOI
Marmur A. 2006. Underwater superhydrophobicity: theoretical feasibility. Langmuir 22, 1400–1402. (10.1021/la052802j) PubMed DOI
Bormashenko E. 2010. Wetting transitions on biomimetic surfaces. Phil. Trans. R. Soc. A 368, 4695–4711. (10.1098/rsta.2010.0121) PubMed DOI
McHale G, Shirtcliffe NJ, Newton MI. 2004. Contact-angle hysteresis on super-hydrophobic surfaces. Langmuir 20, 10 146–10 149. (10.1021/la0486584) PubMed DOI
Reyssat M, Quéré D. 2009. Contact angle hysteresis generated by strong dilute defects. J. Phys. Chem. B 113, 3906–3909. (10.1021/jp8066876) PubMed DOI
Fincke OM. 1986. Underwater oviposition in a damselfly (Odonata, Coenagrionidae) favors male vigilance and multiple mating by females. Behav. Ecol. Sociobiol. 18, 405–412. (10.1007/BF00300514) DOI
Spence JR. 1986. Interactions between the scelionid egg parasitoid Tiphodytes gerriphagus (Hymenoptera) and its gerrid hosts (Heteroptera). Can. J. Zool. 64, 2728–2738. (10.1139/z86-397) DOI
Miller PL. 1994. The effect of oxygen lack on egg hatching in an Indian dragonfly, Potamarcha congener. Physiol. Entomol. 17, 68–72. (10.1111/j.1365-3032.1992.tb00991.x) DOI
Harabiš F, Dolný A, Helebrandová J, Rusková T. 2015. Do egg parasitoids increase the tendency of Lestes sponsa (Odonata: Lestidae) to oviposit underwater? Eur. J. Entomol. 112, 63–68. (10.14411/eje.2015.017) DOI
Robert PA. 1958. Les libellules (Odonates). Neuchâtel, France: Delachaux et Niestlé.
Helebrandová JB, Pyszko P, Dolný A. 2019. Behavioural phenotypic plasticity of submerged oviposition in damselflies (Insecta: Odonata). Insects 10, 124 (10.3390/insects10050124) PubMed DOI PMC
Sun M, Chen Y, Zheng Y, Zhen M, Shu C, Dai Z, Liang A, Gorb SN. 2017. Wettability gradient on the elytra in the aquatic beetle Cybister chinensis and its role in angular position of the beetle at water-air interface. Acta Biomater. 51, 408–417. (10.1016/j.actbio.2017.01.022) PubMed DOI
Parker AR, Lawrence CR. 2001. Water capture by a desert beetle. Nature 414, 33–34. (10.1038/35102108) PubMed DOI
Fang Y, Sun G, Bi Y, Zhi H. 2015. Multiple-dimensional micro/nano structural models for hydrophobicity of butterfly wing surfaces and coupling mechanism. Sci. Bull. 60, 256–263. (10.1007/s11434-014-0653-3) DOI
Blossey R. 2003. Self-cleaning surfaces—virtual realities. Nat. Mater. 2, 301–306. (10.1038/nmat856) PubMed DOI
Fürstner R, Barthlott W, Neinhuis C, Walzel P. 2005. Wetting and self-cleaning properties of artificial superhydrophobic surfaces. Langmuir 21, 956–961. (10.1021/la0401011) PubMed DOI
Bhushan B, Jung YC. 2011. Natural and biomimetic artificial surfaces for superhydrophobicity, self-cleaning, low adhesion, and drag reduction. Prog. Mater. Sci. 56, 1–108. (10.1016/j.pmatsci.2010.04.003) DOI
McCauley SJ. 2007. The role of local and regional processes in structuring larval dragonfly distributions across habitat gradients. Oikos 116, 121–133. (10.1111/j.2006.0030-1299.15105.x) DOI
Norberg RÅ. 1972. The pterostigma of insect wings an inertial regulator of wing pitch. J. Comp. Physiol. 81, 9–22. (10.1007/BF00693547) DOI
Wootton RJ. 1991. The functional morphology of the wings of Odonata. Adv. Odonatol. 5, 153–169.
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