Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

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.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Abramowitz M, Stegun IA (1965) Handbook of mathematical functions. National Bureau of Standards. Appl Math. Series 55. Dover Publications, USA

  • 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 59:752–761

    Article  PubMed  Google Scholar 

  • Bacon JP, Murphey RK (1984) Receptive fields of cricket giant interneurons are related to their dendritic structure. J Physiol 352:601–623

    PubMed  CAS  Google Scholar 

  • Bailey TC, Gatrell AC (1995) Interactive spatial data analysis. Wiley, NY, USA

    Google Scholar 

  • Barth FG (2001) A spider’s world: senses and behavior. Springer, Berlin

    Google Scholar 

  • 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 191:733–746

    Article  Google Scholar 

  • Butler AB, Hodos W (2005) Comparative vertebrate neuroanatomy: evolution and adaptation. Wiley, NY

    Google Scholar 

  • 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 128:203–212

    Article  Google Scholar 

  • 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 203:3279–3287

    PubMed  CAS  Google Scholar 

  • 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 387:215–233

    Article  PubMed  CAS  Google Scholar 

  • Cummins B, Gedeon T, Klapper I, Cortez R (2007) Interaction between arthropod filiform hairs in a fluid environment. J Theor Biol 247:266–80

    Article  PubMed  Google Scholar 

  • Dangles O, Pierre D, Magal C, Vannier F, Casas J (2006) Ontogeny of air-motion sensing in cricket. J Exp Biol 209:4363–4370

    Article  PubMed  CAS  Google Scholar 

  • Diggle PJ (1983) Statistical analysis of spatial point patterns. Academic Press, London, UK

    Google Scholar 

  • 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 185:83–103

    Article  PubMed  CAS  Google Scholar 

  • 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 1–92

    Google Scholar 

  • Gnatzy W, Kämper G (1990) Digger wasps against crickets. II. An airborne signal produced by a running predator. J Comp Physiol A 167:551–556

    Article  Google Scholar 

  • 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 213:441–463

    PubMed  CAS  Google Scholar 

  • Holtsmark J, Johnsen I, Sikkeland T, Skavlem S (1954) Boundary layer flow near a cylindrical obstacle in oscillating, incompressible fluid. J Acoust Soc Am 26:26–39

    Article  Google Scholar 

  • Horridge GA, Duelli P (1979) Anatomy of the regional differences in the eye of the mantis Ciulfina. J Exp Biol 80:165–190

    Google Scholar 

  • 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 1–80

  • 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 340:423–444

    Article  Google Scholar 

  • 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 129–144

    Google Scholar 

  • Jacobs GA, Theunissen FE (1996) Functional organization of a neural map in the cricket cercal sensory system. J Neurosci 16:769–784

    PubMed  CAS  Google Scholar 

  • 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 294:1948–1951

    Article  PubMed  CAS  Google Scholar 

  • Landolfa MA, Jacobs GA (1995) Direction sensitivity of the filiform hair population of the cricket cercal system. J Comp Physiol A 177:759–766

    Google Scholar 

  • Lim DJ (1986) Functional structure of the organ of Corti: a review. Hearing Res 22:117–146

    Article  CAS  Google Scholar 

  • Magal C, Dangles O, Caparroy P, Casas J (2006) Hair canopy of cricket sensory system tuned to predator signals. J Theor Biol 241:459–466

    Article  PubMed  Google Scholar 

  • Manley GA, Popper AN, Fay RR (2004) Evolution of the vertebrate auditory system (Springer handbook of auditory research). Springer, Berlin

    Google Scholar 

  • Mayinger F, Feldman O (2001) Optical measurements: techniques and applications, 2nd edn. Springer, Berlin

    Google Scholar 

  • Merzkirch W (2001) Particle image velocimetry. In: Mayinger F, Feldmann O (eds) Optical measurements techniques and applications. Springer, Berlin, pp 337–353

    Google Scholar 

  • Moller AR (2002) Sensory systems: anatomy and physiology. Academic Press, London

    Google Scholar 

  • Osborne LC (1996) Signal processing in a mechanosensory array: dynamic of cricket cercal hairs. PhD Thesis, University of California

  • Palka J, Olberg R (1977) The cercus-to-giant interneuron system of crickets. III. Receptive field organization. J Comp Physiol A 119:301–317

    Article  Google Scholar 

  • 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 1157

  • Shimozawa T, Kanou M (1984a) Varieties of filiform hairs: range fractionation by sensory afferents and cercal interneurons of a cricket. J Comp Physiol A 155:485–493

    Article  Google Scholar 

  • 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 155:495–505

    Article  Google Scholar 

  • 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 145–157

    Google Scholar 

  • Smith CUM (2000) Biology of sensory systems. Wiley, Hoboken

    Google Scholar 

  • Steinmann T, Casas J, Krijnen G, Dangles O (2006) Air-flow sensitive hairs: boundary layers in oscillatory flows around arthropod appendages. J Exp Biol 209:4398–4408

    Article  PubMed  CAS  Google Scholar 

  • Tautz J, Markl H (1978) Caterpillars detect flying wasps by hairs sensitive to airborne vibration. Behav Ecol Sociobiol 4:101–110

    Article  Google Scholar 

  • Van Lieshout MNM, Baddeley AJ (1999) Indices of dependence between types in multivariate point patterns. Scand J Stat 26:511–532

    Article  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, Berlin

    Google Scholar 

  • Walthall WW, Murphey RK (1986) Positional information, compartments, and the cercal sensory system of crickets. Dev Biol 113:182–200

    Article  Google Scholar 

  • Wang YW (1968) On high-frequency oscillatory viscous flows. J Fluid Mechan 32:55–68

    Article  Google Scholar 

  • Yost WA (2000) Fundamentals of hearing: an introduction. Academic Press, London, UK

    Google Scholar 

  • Zar JH (1998) Biostatistical analysis. Prentice Hall, New York

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Université de Tours, IRBI UMR CNRS 6035, Parc Grandmont, 37200, Tours, France

    Olivier Dangles, Thomas Steinmann, Dominique Pierre, Fabrice Vannier & Jérôme Casas

  2. IRD, UR 072, Laboratoire Evolution, Génomes et Spéciation, UPR 9034, CNRS, 91198, Gif-sur-Yvette Cedex, France

    Olivier Dangles

  3. Université Paris-Sud 11, 91405, Orsay Cedex, France

    Olivier Dangles

Authors
  1. Olivier Dangles
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas Steinmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dominique Pierre
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fabrice Vannier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jérôme Casas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jérôme Casas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dangles, O., Steinmann, T., Pierre, D. et al. Relative contributions of organ shape and receptor arrangement to the design of cricket’s cercal system. J Comp Physiol A 194, 653–663 (2008). https://doi.org/10.1007/s00359-008-0339-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-008-0339-x

Keywords

Search

Navigation