Advertisement

Relative contributions of organ shape and receptor arrangement to the design of cricket’s cercal system

  • Olivier Dangles
  • Thomas Steinmann
  • Dominique Pierre
  • Fabrice Vannier
  • Jérôme Casas
Original Paper

Abstract

Understanding the relative contributions of the shape of a sensory organ and the arrangement of receptors to the overall performance of the organ has long been a challenge for sensory biologists. We tackled this issue using the wind-sensing system of crickets, the cerci, two conical abdominal appendages covered with arrays of filiform hairs. Scanning electron microscopy coupled with 3D reconstruction methods were used for mapping of all cercal filiform hairs. The hairs are arranged according to their diameter in a way that avoids collisions with neighbours during hair deflection: long hairs are regularly spaced, whereas short hairs are both randomly and densely distributed. Particle image velocimetry showed that the variation in diameter of the cercus along its length modifies the pattern of fluid velocities. Hairs are subject to higher air flow amplitudes at the base than at the apex of the cercus. The relative importance of interactions between receptors and the air flow around the organ may explain the performance of the cricket’s cercal system: it is characterised by a high density of statistically non-interacting short hairs located at the base of the cercus where sensitivity to air currents is the highest.

Keywords

Air sensing Sensory ecology Particle image velocimetry Point pattern analysis Sensory hair arrays 

Notes

Acknowledgments

The authors thank two anonymous reviewers and Gijs Krijnen for their constructive comments on the first version of this manuscript. They also thank Philippe Caparroy for his help in the three-dimensional reconstitution of the cercus surface. This work is part of the research conducted within the Cricket Inspired perCeption and Autonomous Decision Automata (CICADA) project (IST-2001-34718) and within the Customized Intelligent Life Inspired Arrays (CILIA) project (FP6-IST-016039). These projects are both funded by the European Community under the “Information Society Technologies–IST” Program, Future and emergent Technologies (FET), Lifelike Perception Systems action.

References

  1. Abramowitz M, Stegun IA (1965) Handbook of mathematical functions. National Bureau of Standards. Appl Math. Series 55. Dover Publications, USAGoogle Scholar
  2. Apanasovich TV, Sheather S, Lupton JR, Popovic N, Tuner ND, Chapkin RS, Braby LA, Carroll RJ (2003) Testing for spatial correlation in nonstationary binary data, with application to aberrant crypt foci in colon carcinogenesis. Biometrics 59:752–761PubMedCrossRefGoogle Scholar
  3. Bacon JP, Murphey RK (1984) Receptive fields of cricket giant interneurons are related to their dendritic structure. J Physiol 352:601–623PubMedGoogle Scholar
  4. Bailey TC, Gatrell AC (1995) Interactive spatial data analysis. Wiley, NY, USAGoogle Scholar
  5. Barth FG (2001) A spider’s world: senses and behavior. Springer, BerlinGoogle Scholar
  6. Bathellier B, Barth FG, Albert JT, Humphrey JAC (2005) Viscosity-mediated motion coupling between pairs of trichobothria on the leg of the spider Cupiennius salei. J Comp Physiol A 191:733–746CrossRefGoogle Scholar
  7. Butler AB, Hodos W (2005) Comparative vertebrate neuroanatomy: evolution and adaptation. Wiley, NYGoogle Scholar
  8. Camhi JM, Tom W, Volman S (1978) The escape behavior of the cockroach Periplaneta Americana. II. Detection of natural predators by air displacement. J Comp Physiol A 128:203–212CrossRefGoogle Scholar
  9. Castello ME, Aguilera PA, Trujillo-Cenoz O, Caputi AA (2000) Eletroreception in Gymnotus carapo : pre-receptor processing and the distribution of electroreceptor types. J Exp Biol 203:3279–3287PubMedGoogle Scholar
  10. Catania KC, Kaas JH (1997) Somatosensory fovea in the star-nosed mole: behavioural use of the star in relation to innervation patterns and cortical representation. J Comp Neurol 387:215–233PubMedCrossRefGoogle Scholar
  11. Cummins B, Gedeon T, Klapper I, Cortez R (2007) Interaction between arthropod filiform hairs in a fluid environment. J Theor Biol 247:266–80PubMedCrossRefGoogle Scholar
  12. Dangles O, Pierre D, Magal C, Vannier F, Casas J (2006) Ontogeny of air-motion sensing in cricket. J Exp Biol 209:4363–4370PubMedCrossRefGoogle Scholar
  13. Diggle PJ (1983) Statistical analysis of spatial point patterns. Academic Press, London, UKGoogle Scholar
  14. Edwards JS, Palka J (1974) The cerci and abdominal giant fibres of the house cricket Acheta domesticus. I. Anatomy and physiology of normal adults. Proc R Soc Lond B 185:83–103PubMedCrossRefGoogle Scholar
  15. Gnatzy W (1996) Digger wasp vs. cricket: neuroethology of a predator–prey interaction. In: Lindauer M (ed) Information processing in animals, vol 10. Fischer-Verlag, Stuttgart, pp 1–92Google Scholar
  16. Gnatzy W, Kämper G (1990) Digger wasps against crickets. II. An airborne signal produced by a running predator. J Comp Physiol A 167:551–556CrossRefGoogle Scholar
  17. Gnatzy W, Tautz J (1980) Ultrastructure and mechanical properties of an insect mechanoreceptor. Stimulus-transmitting structures and sensory apparatus of the cercal filiform hairs of Gryllus. Cell Tissue Res 213:441–463PubMedGoogle Scholar
  18. Holtsmark J, Johnsen I, Sikkeland T, Skavlem S (1954) Boundary layer flow near a cylindrical obstacle in oscillating, incompressible fluid. J Acoust Soc Am 26:26–39CrossRefGoogle Scholar
  19. Horridge GA, Duelli P (1979) Anatomy of the regional differences in the eye of the mantis Ciulfina. J Exp Biol 80:165–190Google Scholar
  20. Humphrey JAC, Barth FG (2007) Medium flow-sensing hairs: biomechanics and models. In: Casas J, Simpson SJ (eds) Insect mechanics and control: adv insect physiol, vol 34, pp 1–80Google Scholar
  21. Humphrey JAC, Devarakonda R, Iglesias I, Barth FG (1993) Dynamics of Arthropod filiform hairs. I. Mathematical modelling of the hair and air motions. Phil Trans R Soc Lond B 340:423–444CrossRefGoogle Scholar
  22. Humphrey JAC, Barth FG, Reed M, Spak A (2003) The physics of arthropod medium-flow sensitive hairs: biological models for artificial sensors. In: Barth FG, Humphrey JAC, Secomb T (eds) Sensors and sensing in biology and engineering. Springer, Berlin, pp 129–144Google Scholar
  23. Jacobs GA, Theunissen FE (1996) Functional organization of a neural map in the cricket cercal sensory system. J Neurosci 16:769–784PubMedGoogle Scholar
  24. Koehl MAR, Koseff JR, Crimaldi JP, McCay MG, Cooper T, Wiley MB, Moore PA (2001) Lobster sniffing: antennule design and hydrodynamic filtering of information in an odour plume. Science 294:1948–1951PubMedCrossRefGoogle Scholar
  25. Landolfa MA, Jacobs GA (1995) Direction sensitivity of the filiform hair population of the cricket cercal system. J Comp Physiol A 177:759–766Google Scholar
  26. Lim DJ (1986) Functional structure of the organ of Corti: a review. Hearing Res 22:117–146CrossRefGoogle Scholar
  27. Magal C, Dangles O, Caparroy P, Casas J (2006) Hair canopy of cricket sensory system tuned to predator signals. J Theor Biol 241:459–466PubMedCrossRefGoogle Scholar
  28. Manley GA, Popper AN, Fay RR (2004) Evolution of the vertebrate auditory system (Springer handbook of auditory research). Springer, BerlinGoogle Scholar
  29. Mayinger F, Feldman O (2001) Optical measurements: techniques and applications, 2nd edn. Springer, BerlinGoogle Scholar
  30. Merzkirch W (2001) Particle image velocimetry. In: Mayinger F, Feldmann O (eds) Optical measurements techniques and applications. Springer, Berlin, pp 337–353Google Scholar
  31. Moller AR (2002) Sensory systems: anatomy and physiology. Academic Press, LondonGoogle Scholar
  32. Osborne LC (1996) Signal processing in a mechanosensory array: dynamic of cricket cercal hairs. PhD Thesis, University of CaliforniaGoogle Scholar
  33. Palka J, Olberg R (1977) The cercus-to-giant interneuron system of crickets. III. Receptive field organization. J Comp Physiol A 119:301–317CrossRefGoogle Scholar
  34. Schram C, Riethmuller ML (2001) Evolution of vortex ring characteristics during pairing in an acoustically excited jet using stroboscopic particle image velocimetry. In: 4th international symposium on particle image velocimetry (PIV’01), Göttingen, 17–19 September, paper 1157Google Scholar
  35. Shimozawa T, Kanou M (1984a) Varieties of filiform hairs: range fractionation by sensory afferents and cercal interneurons of a cricket. J Comp Physiol A 155:485–493CrossRefGoogle Scholar
  36. Shimozawa T, Kanou M (1984b) The aerodynamics and sensory physiology of range fractionation in the cercal filiform sensilla of the cricket Gryllus bimaculatus. J Comp Physiol A 155:495–505CrossRefGoogle Scholar
  37. Shimozawa T, Murakami J, Kumagai T (2003) Cricket wind receptors: thermal noise for the highest sensitivity known. In: Barth FG, Humphrey JAC, Secomb T (eds) Sensors and sensing in biology and engineering. Springer, Berlin, pp 145–157Google Scholar
  38. Smith CUM (2000) Biology of sensory systems. Wiley, HobokenGoogle Scholar
  39. Steinmann T, Casas J, Krijnen G, Dangles O (2006) Air-flow sensitive hairs: boundary layers in oscillatory flows around arthropod appendages. J Exp Biol 209:4398–4408PubMedCrossRefGoogle Scholar
  40. Tautz J, Markl H (1978) Caterpillars detect flying wasps by hairs sensitive to airborne vibration. Behav Ecol Sociobiol 4:101–110CrossRefGoogle Scholar
  41. Van Lieshout MNM, Baddeley AJ (1999) Indices of dependence between types in multivariate point patterns. Scand J Stat 26:511–532CrossRefGoogle Scholar
  42. Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, BerlinGoogle Scholar
  43. Walthall WW, Murphey RK (1986) Positional information, compartments, and the cercal sensory system of crickets. Dev Biol 113:182–200CrossRefGoogle Scholar
  44. Wang YW (1968) On high-frequency oscillatory viscous flows. J Fluid Mechan 32:55–68CrossRefGoogle Scholar
  45. Yost WA (2000) Fundamentals of hearing: an introduction. Academic Press, London, UKGoogle Scholar
  46. Zar JH (1998) Biostatistical analysis. Prentice Hall, New YorkGoogle Scholar

Copyright information

© Springer Verlag 2008

Authors and Affiliations

  • Olivier Dangles
    • 1
    • 2
    • 3
  • Thomas Steinmann
    • 1
  • Dominique Pierre
    • 1
  • Fabrice Vannier
    • 1
  • Jérôme Casas
    • 1
  1. 1.Université de Tours, IRBI UMR CNRS 6035ToursFrance
  2. 2.IRD, UR 072, Laboratoire Evolution, Génomes et Spéciation, UPR 9034, CNRSGif-sur-Yvette CedexFrance
  3. 3.Université Paris-Sud 11Orsay CedexFrance

Personalised recommendations