Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-19T15:12:10.889Z Has data issue: false hasContentIssue false

Underwater breathing: the mechanics of plastron respiration

Published online by Cambridge University Press:  11 July 2008

M. R. FLYNN
Affiliation:
Department of Mathematics, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139-4307, USA
JOHN W. M. BUSH
Affiliation:
Department of Mathematics, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139-4307, USA

Abstract

The rough, hairy surfaces of many insects and spiders serve to render them water-repellent; consequently, when submerged, many are able to survive by virtue of a thin air layer trapped along their exteriors. The diffusion of dissolved oxygen from the ambient water may allow this layer to function as a respiratory bubble or ‘plastron’, and so enable certain species to remain underwater indefinitely. Maintenance of the plastron requires that the curvature pressure balance the pressure difference between the plastron and ambient. Moreover, viable plastrons must be of sufficient area to accommodate the interfacial exchange of O2 and CO2 necessary to meet metabolic demands. By coupling the bubble mechanics, surface and gas-phase chemistry, we enumerate criteria for plastron viability and thereby deduce the range of environmental conditions and dive depths over which plastron breathers can survive. The influence of an external flow on plastron breathing is also examined. Dynamic pressure may become significant for respiration in fast-flowing, shallow and well-aerated streams. Moreover, flow effects are generally significant because they sharpen chemical gradients and so enhance mass transfer across the plastron interface. Modelling this process provides a rationale for the ventilation movements documented in the biology literature, whereby arthropods enhance plastron respiration by flapping their limbs or antennae. Biomimetic implications of our results are discussed.

Type
Papers
Copyright
Copyright © Cambridge University Press 2008

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.)

References

REFERENCES

Abdelsalam, M. E., Bartlett, P. N., Kelf, T. & Baumberg, J. 2005 Wetting of regularly structured gold surfaces. Langmuir 21, 17531757.CrossRefGoogle ScholarPubMed
Andersen, N. M. 1976 A comparative study of locomotion on the water surface in semiaquatic bugs (Insects, Hemiptera, Gerromorpha). Vidensk. Meddr. Dansk. Naturh. Foren. 139, 337396.Google Scholar
Andersen, N. M. 1977 Fine structure of the body hair layers and morphology of the spiracles of semiaquatic bugs (Insecta, Hemiptera, Gerromorpha) in relation to life on the water surface. Vidensk. Meddr. Dansk. Naturh. Foren. 140, 737.Google Scholar
Andersen, N. M. & Polhemus, J. T. 1976 Water-striders (Hemiptera: Gerridae, Veliidae, etc.). In Marine Insects (ed. Cheng, L.), pp. 187–224. A North Holland.Google Scholar
Barthlott, W. & Neinhuis, C. 1997 Purity of the sacred lotus, or escape from contamination in biological surfaces. Planta 202, 18.CrossRefGoogle Scholar
Bico, J., Roman, B., Moulin, L. & Boudaoud, A. 2004 Elastocapillary coalescence in wet hair. Nature 432, 690.CrossRefGoogle ScholarPubMed
Bico, J., Thiele, U. & Quérée, D. 2002 Wetting of textured surfaces. Colloids Surf. A 206, 4146.CrossRefGoogle Scholar
Brocher, F. 1912 a Reserches sur la respiration des insects aquatiques adultes – les elmides. Ann. Biol. Lac. 5, 136179.Google Scholar
Brocher, F. 1912 b Reserches sur la respiration des insects aquatiques adultes – les haemonia. Ann. Biol. Lac. 5, 526.Google Scholar
Brown, H. P. 1987 Biology of riffle beetles. Annu. Rev. Entomol. 32, 253273.CrossRefGoogle Scholar
Bush, J. W. M. & Hu, D. L. 2006 Walking on water: Biolocomotion at the interface. Annu. Rev. Fluid Mech. 38, 339369.CrossRefGoogle Scholar
Bush, J. W. M., Hu, D. L. & Prakash, M. 2008 The integument of water-walking anthropods: Form and function. Adv. Insect Physiol. 34, 117192.Google Scholar
Cao, L., Hu, H.-H. & Gao, D. 2007 Design and fabrication of mirco-textures for inducing a superhydrophobic behavior on hydrophilic materials. Langmuir 23, 43104314.CrossRefGoogle ScholarPubMed
Carbone, G. & Mangialardi, L. 2005 Hydrophobic properties of a wavy rough substrate. Eur. Phys. J. E 16, 6776.Google ScholarPubMed
Cassie, A. B. D. & Baxter, S. 1944 Wettability of porous surfaces. Trans. Faraday Soc. 40, 546551.CrossRefGoogle Scholar
Chaui-Berlinck, J. G., Bicudo, J. E. & Monteiro, L. H. 2001 The oxygen gain of diving insects. Respir. Physiol. 128, 229233.CrossRefGoogle ScholarPubMed
Chen, Y., He, B., Lee, J. & Patankar, N. A. 2005 Anisotropy in the wetting of rough surfaces. J. Colloid Interface Sci. 281, 458464.CrossRefGoogle ScholarPubMed
Couzin, I. D. & Krause, J. 2003 Self-organization and collective behavior in vertebrates. J. Adv. Study Behav. 32, 175.Google Scholar
Crisp, D. J. 1949 The stability of structures at a fluid interface. Trans. Faraday Soc. 46, 228235.CrossRefGoogle Scholar
Dokulil, M. T. 2005 European alpine lakes. In The Lake Handbook(ed. O'Sullivan, P. E. & Reynolds, C. S.), vol. 2, pp. 159178. Blackwell.Google Scholar
Doyen, J. T. 1976 Marine beetles (Coleoptera excluding Staphylinidae). In Aquatic Insects (ed. Cheng, L.), pp. 497520. North-Holland.Google Scholar
Ege, R. 1918 On the respiratory function of the air stores carried by some aquatic insects. Z. Allg. Physiol. 17, 81124.Google Scholar
Feng, Xi-Qiao & Jiang, Lei 2006 Design and creation of superwetting/antiwetting surfaces. Adv. Mater. 18, 30633078.CrossRefGoogle Scholar
Geankoplis, C. J. 1993 Transport Processes and Unit Operations. Prentice Hall.Google Scholar
de Gennes, P G, Brochard-Wyart, F & Quéré, D 2003 Capillarity and Wetting Phenomena: Drops, Bubbles, Pearls and Waves. Springer.Google Scholar
Gittelman, S. H. 1975 Physical gill efficiency and water dormancy in the pigmy backswimmer, Neoplea striola (Hemiptera: Pleidae). Ann. Entomolo. Soc. Am. 68, 10111017.CrossRefGoogle Scholar
Herminghaus, S. 2000 Roughness-induced non-wetting. Europhys. Lett. 52, 165170.CrossRefGoogle Scholar
Hinton, H. E. 1976 Plastron respiration in bugs and beetles. J. Insect Physiol. 22, 15291550.CrossRefGoogle Scholar
Hinton, H. E. & Jarman, G. M. 1976 A diffusion equation for tapered plastrons. J. Insect Physiol. 22, 12631265.CrossRefGoogle Scholar
Holdgate, M. W. 1955 The wetting of insect cuticle by water. J. Expl Biol. 32, 591617.CrossRefGoogle Scholar
Kim, H.-Y. & Mahadevan, L. 2006 Capillary rise between elastic sheets. J. Fluid Mech. 548, 141150.CrossRefGoogle Scholar
Kralchevsky, P. A. & Denkov, N. D. 2001 Capillary forces and structuring in layers of colloid particles. Curr. Opin. Colloid Interface Sci. 6, 383401.Google Scholar
Kundu, P. K. 1990 Fluid Mechanics, 1st edn. Academic.Google Scholar
Lafuma, A. & Quéré, D. 2003 Superhydrophobic states. Nature Materials 2, 457460.Google Scholar
Lamoral, B. H. 1968 On the ecology and habitat adaptations of two intertidal spiders, Desis formidabilis and Amaurobioides africanus Hewitt at ‘The Ísland’ (Kommetjie, Cape Peninsula) with notes on the occurence of two other spiders. Annu. Natal. Mus. 20, 151193.Google Scholar
Linden, P. F. 1999 The fluid mechanics of natural ventilation. Annu. Rev. Fluid Mech. 31, 201238.CrossRefGoogle Scholar
Matthews, P. G. D. & Seymour, R. S. 2006 Diving insects boost their buoyancy bubbles. Nature 441, 171.Google Scholar
McMahon, T. & Bonner, J. T. 1985 On Size and Life. W. H. Freeman & Co.Google Scholar
Neinhuis, C. & Barthlott, W. 1997 Characterization and distribution of water-repellent, self-cleaning plant surfaces. Annu. Bot. 79, 667677.Google Scholar
Nosonovsky, M. 2007 Multiscale roughness and stability of superhydrophobic biomimetic interfaces. Langmuir 23, 31573161.CrossRefGoogle ScholarPubMed
Otten, A. & Herminghaus, S. 2004 How plants keep dry: A physicist's point of view. Langmuir 20, 24052408.Google Scholar
Perez-Goodwyn, P. J. 2007 Anti-wetting surfaces in Heteroptera (Insecta): Hairy solutions to any problem. In Functional Surfaces in Biology. Springer.Google Scholar
Rahn, H. & Paganelli, C. V. 1968 Gas exchange in gas gills of diving insects. Respir. Physiol. 5, 145164.CrossRefGoogle ScholarPubMed
Reysatt, M., Yeomans, J. M. & Quéré, D. 2008 Implacement of fakir drops. Europhys. Lett. 81, 26006.CrossRefGoogle Scholar
Reyssat, M. C. 2007 Splendeur et misére de l'effet lotus. PhD thesis, Université Pierre et Marie Curie.Google Scholar
de Ruiter, L., Wolvekamp, H. P., van Tooren, A. J. & Vlasblom, A. 1951 Experiments on the efficiency of the “physical gill” (Hydrous piceus l., Naucoris cimicoides l., and Notonecta glauca l.). Acta Physiol. Pharmacol. Neerl. pp. 180–213.Google Scholar
Schmidt-Nielsen, K. 1975 Animal Physiology – Adaptation and Environment. Cambridge University Press.Google Scholar
Schütz, D. & Taborsky, M. 2003 Adaptations to an aquatic life may be responsible for the reversed sexual size dimorphism in the water spider, argyroneta aquatica. Ecol. Evol. Res. 5, 105117.Google Scholar
Shirtcliffe, N. J., McHale, G., Newton, M. I., Perry, C. C. & Pyatt, F. Brian 2006 Plastron properties of a superhydrophobic surface. Appl. Phys. Lett. 89, 104106.Google Scholar
Spence, J. R., Spence, D. H. & Scudder, G. G. 1980 Submergence behavior in Gerris: Underwater basking. Am. Midl. Nat. 103, 385391.Google Scholar
Stratton, G. E., Suter, R. B. & Miller, P. R. 2004 Evolution of water surface locomotion by spiders: a comparative approach. Biol. J. Linn. Soc. 81 (1), 6378.Google Scholar
Stride, G. O. 1954 On the respiration of an aquatic african beetle, Potamodytes tuberosus Hinton. Ann. Entomolo. Soc. Am. 48, 344351.Google Scholar
Thorpe, W. H. 1950 Plastron respiration in aquatic insects. Biol. Rev. 25, 344390.CrossRefGoogle ScholarPubMed
Thorpe, W. H. & Crisp, D. J. 1947 a Studies on plastron respiration. Part I. The biology of Aphelocheirus [Hemiptera, Aphelocheiridae (Naucoridae)] and the mechanism of plastron retention. J. Expl Biol. 24, 227269.Google Scholar
Thorpe, W. H. & Crisp, D. J. 1947 b Studies on plastron respiration. Part II. The respiratory efficiency of the plastron in Aphelocheirus. J. Expl Biol. 24, 270303.CrossRefGoogle Scholar
Thorpe, W. H. & Crisp, D. J. 1947 c Studies on plastron respiration. Part III. The orientation responses of Aphelocheirus [Hemiptera, Aphelocheiridae (Naucoridae)] in relation to plastron respiration; together with an account of specialized pressure receptors in aquatic insects. J. Expl Biol. 24, 310328.CrossRefGoogle Scholar
Thorpe, W. H. & Crisp, D. J. 1949 Studies on plastron respiration. Part IV. Plastron respiration in the Coleoptera. J. Expl Biol. 26, 219260.CrossRefGoogle Scholar
Vogel, S. 2006 Living in a physical world viii. Gravity and life in the water. J. Biosci. 31, 309322.CrossRefGoogle Scholar
Wagner, P, Furstner, R, Barthlott, W & Neinhuis, C 2003 Quantitative assessment to the structural basis of water repellency in natural and technical surfaces. J. Expl Bot. 54, 12951303.CrossRefGoogle Scholar
Wenzel, R. N. 1936 Resistance of solid surfaces to wetting by water. Ind. Engng Chem. 28, 988994.CrossRefGoogle Scholar