Advertisement

The Slightest Whiff of Air: Airflow Sensing in Arthropods

  • Friedrich G. BarthEmail author
Chapter

Abstract

The perception of medium flows has received ever increasing attention during the last two decades and has increasingly been recognized as a sensory capacity of its own. A combination of experimental work and physical–mathematical modeling has deepened our understanding of the workings of airflow sensors, mainly represented by insect filiform hairs and arachnid trichobothria, both as individual sensors and sensor arrays. This chapter points to the diversity of arthropod airflow sensors and stresses the importance of comparative studies. These should include animal groups so far largely neglected by sensory biology and neuroethology. Another need is to analyze biologically relevant flow patterns and to relate these to the functional properties of the various patterns of sensor arrangement found in different animal taxa. Finally, the capture of a freely flying fly by a wandering spider is taken to illustrate the challenges and promises of studies that aim to reveal the relation between a particular airflow pattern and a specific behavior.

Keywords

High Frequency Component Medium Flow Oribatid Mite Hair Shaft Digital Particle Image Velocimetry 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The author’s research and that of his associates was generously supported by the DARPA BIOsenSE program grant no. FA9550-05-1-0459 and by several earlier grants of the Austrian Science Fund, FWF. The kind help of Clemens Schaber with the preparation of the figures is gratefully acknowledged.

References

  1. Albert JT, Friedrich OC, Dechant H-E, Barth FG (2001) Arthropod touch reception: spider hair sensilla as rapid touch detectors. J Comp Physiol A 187:303–312PubMedCrossRefGoogle Scholar
  2. Alberti G, Moreno AI, Kratzmann M (1994) The fine structure of trichobothria in moss mites with special emphasis on Acrogalumna longipluma (Berlese, 1904) (Oribatida, Acari, Arachnida). Acta Zool (Stockholm) 75(1):57–74CrossRefGoogle Scholar
  3. Altner H (1977) Insect sensillum specificity and structure: an approach to a new typology. In: LeMagnen J, MacLeod P (eds) Olfaction and taste, vol VI., Paris Information retrieval, London, Washington DC, pp 295–303Google Scholar
  4. Anton S (1991) Zentrale Projektionen von Mechano- und Chemoreceptoren bei der Jagdspinne Cupiennius salei Keys. Doctoral thesis, University of ViennaGoogle Scholar
  5. Barth FG (1997) Vibratory communication in spiders: adaptation and compromise at many levels. In: Lehrer M (ed) Orientation and communication in arthropods. Birkhäuser, pp 247–272Google Scholar
  6. Barth FG (2002) A spider’s world: senses and behavior. Trichobothria: the measurement of air movement, Chap. IX. Springer, Berlin Heidelberg, pp 85–109Google Scholar
  7. Barth FG, Dechant H-E (2003) Arthropod cuticular hairs: tactile sensors and the refinement of stimulus transformation. In: Barth FG, Humphrey JAC, Secomb TW (eds) Sensors and sensing in biology and engineering. Springer, New York, pp 159–171CrossRefGoogle Scholar
  8. Barth FG, Geethabali (1982) Spider vibration receptors: threshold curves of individual slits in the metatarsal lyriform organ. J Comp Physiol A 148:175–185Google Scholar
  9. Barth FG, Höller A (1999) Dynamics of arthropod filiform hairs. V. The response of spider trichobothria to natural stimuli. Phil Trans R Soc Lond B 354:183–192CrossRefGoogle Scholar
  10. Barth FG, Wastl U, Humphrey JAC, Devarakonda R (1993) Dynamics of arthropod filiform hairs. II. Mechanical properties of spider trichobothria (Cupiennius salei Keys.). Phil Trans R Soc Lond B 340:445–461CrossRefGoogle Scholar
  11. Barth FG, Humphrey JAC, Wastl U, Halbritter J, Brittinger W (1995) Dynamics of arthropod filiform hairs. III. Flow patterns related to air movement detection in a spider (Cupiennius salei Keys.). Phil Trans R Soc Lond B 347:397–412CrossRefGoogle Scholar
  12. 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. See also Erratum (2010) J Comp Physiol A 196:89Google Scholar
  13. Bleckmann H (1994) Reception of hydrodynamic stimuli in aquatic and semiaquatic animals. In: Rathmayer W (ed) Progress in Zoology, vol 41. G Fischer, Stuttgart, p 115Google Scholar
  14. Brittinger W (1998) Trichobothrien, Medienströmung und das Verhalten der Jagdspinnen (Cupiennius salei Keys.). Doctoral thesis, University of ViennaGoogle Scholar
  15. Budelmann BU (1989) Hydrodynamic receptor systems in invertebrates. In: Coombs S, Görner P, Münz H (eds) The mechanosensory lateral line: neurobiology and evolution. Springer, New York, pp 607–632CrossRefGoogle Scholar
  16. Camhi J (1984) Neuroethology: nerve cells and the natural behaviour of animals. Sinauer, Sunderland MAGoogle Scholar
  17. Casas J, Dangles O (2010) Physical ecology of fluid flow sensing in arthropods. Annu Rev Entomol 55:505–520PubMedCrossRefGoogle Scholar
  18. Casas J, Steinmann T, Dangles O (2008) The aerodynamic signature of running spiders. PLoS ONE 3(5):e2116 (p 6)Google Scholar
  19. Casas J, Steinmann T, Krijnen G (2010) Why do insects have such a high density of flow-sensing hairs? Insights from the hydromechanics of biomimetic MEMS sensors. J R Soc Interface. doi: 10.1098/rsif.2010.0093 Google Scholar
  20. Cheer AYL, Koehl MAR (1987) Paddles and rakes: fluid flow through bristled appendages of small organisms. J Theor Biol 129:17–39CrossRefGoogle Scholar
  21. Christian UH (1971) Zur Feinstruktur der Trichobothrien der Winkelspinne Tegenaria derhami (Scopoli), (Agelenidae, Araneae). Cytobiologie 4:172–185Google Scholar
  22. Christian UH (1972) Trichobothrien, ein Mechanoreceptor bei Spinnen. Elektronenmikroskopische Befunde bei der Winkelspinne Tegenaria derhami (Scopoli), (Agelenidae, Araneae). Verh Dtsch Zool Ges 66:31–36Google Scholar
  23. Coombs S, Görner P, Münz H (1989) The mechanosensory lateral line: neurobiology and evolution. Springer, New YorkCrossRefGoogle Scholar
  24. Cummins B, Gedeon T (2012) Assessing the mechanical response of groups of arthropod filiform flow sensors. In: Barth FG, Humphrey JAC, Srinivasan MV (eds) Frontiers in sensing from biology to engineering. Springer, New York, pp 239–250CrossRefGoogle Scholar
  25. Cummins B, Gedeon T, Klapper I, Cortez R (2007) Interaction between arthropod filiform hairs in a fluid environment. J Theor Biol 247:266–280PubMedCentralPubMedCrossRefGoogle Scholar
  26. Dangles O, Pierre D, Vannier F, Casas J (2006) Ontogeny of air-motion sensing in cricket. J Exp Biol 209:4363–4370PubMedCrossRefGoogle Scholar
  27. Dechant H-E, Rammerstorfer FG, Barth FG (2001) Arthropod touch reception: stimulus transformation and finite element model of spider tactile hairs. J Comp Physiol A 187:313–322PubMedCrossRefGoogle Scholar
  28. Devarakonda R, Barth FG, Humphrey JAC (1996) Dynamics of arthropod filiform hairs. IV. Hair motion in air and water. Phil Trans R Soc Lond B 351:933–946CrossRefGoogle Scholar
  29. Douglass JK, Wilkens L, Pantazelou E, Moss F (1993) Noise enhancement of information transfer in crayfish mechanoreceptors by stochastic resonance. Nature 365:337–340PubMedCrossRefGoogle Scholar
  30. Draslar K (1973) Functional properties of trichobothria in the bug Pyrrhocoris apterus (L.). J Comp Physiol 84:175–184CrossRefGoogle Scholar
  31. Dumpert K, Gnatzy W (1977) Cricket combined mechanoreceptors and kicking response. J Comp Physiol 122:9–25CrossRefGoogle Scholar
  32. Fenk LM, Hoinkes T, Schmid A (2010) Vision as a third sensory modality to elicit attack behavior in a nocturnal spider. J Comp Physiol A 196:957–961CrossRefGoogle Scholar
  33. Fletcher NH (1978) Acoustical response of hair receptors in insects. J Comp Physiol 127:185–189CrossRefGoogle Scholar
  34. Friedel T, Barth FG (1997) Wind-sensitive interneurons in the spider CNS (Cupiennius salei): directional information processing of sensory inputs from trichobothria on the walking legs. J Comp Physiol A 180:223–233CrossRefGoogle Scholar
  35. Gitter AH, Klinke R (1989) Die Energieschwellen von Auge und Ohr in heutiger Sicht. Naturwissenschaften 76:160–164CrossRefGoogle Scholar
  36. Gnatzy W (1996) Digger wasp vs. cricket: Neuroethology of a predator-prey interaction. In: Lindauer M (ed) Information processing in animals, vol 10. G Fischer, Stuttgart, 92 ppGoogle Scholar
  37. 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
  38. Görner P (1965) A proposed transducing mechanism for a multiply innervated mechanoreceptor (trichobothrium) in spiders. Cold Spring Harbor Symp Quant Biol 30:69–73PubMedCrossRefGoogle Scholar
  39. Görner P, Andrews P (1969) Trichobothrien, ein Ferntastsinnesorgan bei Webspinnen (Araneen). Z vergl Physiol 64:301–317CrossRefGoogle Scholar
  40. Große S, Schröder W (2012) Deflection-based flow field sensors: examples and requirements. In: Barth FG, Humphrey JAC, Srinivasan MV (eds) Frontiers in sensing—from biology to engineering. Springer, New York, pp 393–403CrossRefGoogle Scholar
  41. Harvey MS (1992) The phylogeny and classification of the Pseudoscorpionida (Chelicerata: Arachnida). Invertebr Taxon 6:1373–1435CrossRefGoogle Scholar
  42. Haupt J (1970) Beitrag zur Kenntnis der Sinnesorgane von Symphylen (Myriapoda). I. Elektronenmikroskopische Untersuchung des Trichobothriums von Scutigerella immaculata Newport. Z Zellforsch mikr Anat 110:588–599CrossRefGoogle Scholar
  43. Haupt J (1980) Phylogenetic aspects of recent studies on myriapod sense organs. In: Camatini M (ed) Myriapod biology. Academic Press, London, pp 391–406Google Scholar
  44. Haupt J (1996) Fine structure of the trichobothria and their regeneration during moulting in the whip scorpion Typopeltis crucifer Pocock, 1894. Acta Zool (Stockholm) 77(2):123–136CrossRefGoogle Scholar
  45. Haupt J, Coineau Y (1975) Trichobothrien und Tastborsten der Milbe Microcaeculus (Acari, Prostigmata; Caeculidae). Z Morph Tiere 81:305–322CrossRefGoogle Scholar
  46. Hergenröder R, Barth FG (1983) The release of attack and escape behavior by vibratory stimuli in a wandering spider (Cupiennius salei Keys). J Comp Physiol 152:347–359CrossRefGoogle Scholar
  47. Heys J, Gedeon T, Knott BC, Kim Y (2008) Modeling arthropod hair motion using the penalty immersed boundary layer method. J Biomech Eng 41:977–984Google Scholar
  48. Hoffmann C (1967) Bau und Funktion der Trichobothrien von Euscorpius carpathicus L. Z vergl Physiol 54:290–352CrossRefGoogle Scholar
  49. Humphrey JAC, Barth FG (2008) Medium flow-sensing hairs: biomechanics and models. In: Casas J, Simpson SJ (eds) Insect mechanics and control. Adv Insect Physiol 34:1–81Google Scholar
  50. 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 TW (eds) Sensors and sensing in biology and engineering. Springer, Wien, New York, pp 129–144Google Scholar
  51. Humphrey JAC, Devarakonda R, Iglesias J, Barth FG (1993) Dynamics of arthropod filiform hairs. I. Mathematical modeling of the hair and air motions. Phil Trans R Soc Lond B 340:423–444Google Scholar
  52. Igelmund P (1987) Morphology, sense organs and regeneration of the forelegs (whips) of the whip spider Heterophrynus elaphus (Arachnida, Amblypygi). J Morphol 193:75–89CrossRefGoogle Scholar
  53. Izadi N, Krijnen GJM (2012) Design and fabrication process for artificial lateral line sensors. In: Barth FG, Humphrey JAC, Srinivasan MV (eds) Frontiers in sensing—from biology to engineering. Springer, Wien, New York, pp 405–421CrossRefGoogle Scholar
  54. Judson MLI (2007) A new and endangered pseudoscorpion of the genus Lagynochthonius (Arachnida, Chelonethi, Chthoniidae) from a cave in Vietnam, with notes on chelal morphology and the composition of the Tyrannochthoniini. Zootaxa 1627:53–68Google Scholar
  55. Kant R, Humphrey JAC (2009) Response of cricket and spider motion-sensing hairs to airflow pulsations. J R Soc Interface 6:1047–1064PubMedCentralPubMedCrossRefGoogle Scholar
  56. Klärner D, Barth FG (1982) Vibratory signals and prey capture in orb-weaving spiders (Zygiella x-notata, Nephila clavipes; Araneidae). J Comp Physiol 148:445–455CrossRefGoogle Scholar
  57. Klopsch Ch (2010) The flow field around a flying blowfly: characteristics and guidance of spider prey capture behaviour. Vienna University of Technology, Doctoral thesisGoogle Scholar
  58. Klopsch Ch, Kuhlmann HC, Barth FG (2012) Airflow elicits a spider’s jump towards airborne prey. I. Airflow around a flying blowfly. J R Soc Interface 9:2591–2602. doi: 10.1098/rsif.2012.0186 PubMedCentralPubMedGoogle Scholar
  59. Klopsch Ch, Kuhlmann HC, Barth FG (2013) Airflow elicits a spider’s jump towards airborne prey. II. Flow characteristics guiding behavior. J R Soc Interface 10:82. doi: 10.20120820
  60. 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
  61. Lehtinen PT (1980) Trichobothrial patterns in high level taxonomy of spiders. In: Proceedings of 8th international conference on Arachnol. Egermann, Wien, pp 493–498Google Scholar
  62. Levin JE, Miller JP (1996) Broadband neural encoding in the cricket cercal sensory system enhanced by stochastic resonance. Nature 380:165–168PubMedCrossRefGoogle Scholar
  63. Lewin GC, Hallam J (2010) A computational fluid dynamics model of viscous coupling of hairs. J Comp Physiol A 196:385–395CrossRefGoogle Scholar
  64. Magal C, Dangles O, Caporroy P, Casas J (2006) Hair canopy of cricket sensory system tuned to predator signals. J Theor Biol 241:459–466PubMedCrossRefGoogle Scholar
  65. Mahnert V (1976) Etude comparative des trichobothries de pseudoscorpions au microscope électronique à balayage. CR Séanc Soc Phys Hist Nat 11:96–99Google Scholar
  66. Markl H, Tautz J (1975) The sensitivity of hair receptors in caterpillars of Barathra brassicae L (Lepidoptera, Noctuidae) to particle movement in a sound field. J Comp Physiol 99:79–87CrossRefGoogle Scholar
  67. McConney ME, Tsukruk VV (2012) Synthetic materials for bio-inspired flow-responsive structures. In: Barth FG, Humphrey JAC, Srinivasan MV (eds) Frontiers in sensing—from biology to engineering. Springer, Wien, New York, pp 341–349Google Scholar
  68. McConney ME, Schaber CF, Julian MD, Eberhardt WC, Humphrey JAC, Barth FG, Tsukruk VV (2009) Surface force spectroscopic point load measurements and viscoelastic modelling of the micromechanical properties of air flow sensitive hairs of a spider (Cupiennius salei). J R Soc Interface 6(37):681–694PubMedCentralPubMedCrossRefGoogle Scholar
  69. Messlinger K (1987) Fine structure of scorpion trichobothria (Arachnida, Scorpiones) Zoomorph 107:49–57Google Scholar
  70. Müllan R (2012) Air-flow sensing in Smeringurus mesaensis (Scorpiones: Vaejovidae). Sensor arrangement, behavioral significance and oscillation characteristics of scorpion trichobothria. Doctoral thesis, University of ViennaGoogle Scholar
  71. Nicklaus R (1965) Die Erregung einzelner Fadenhaare von Periplaneta americana in Abhängigkeit von der Größe und Richtung der Auslenkung. Z vergl Physiol 50:331–362CrossRefGoogle Scholar
  72. Peters W, Pfreundt C (1986) Die Verteilung von Trichobothrien und lyraförmigen Organen an den Laufbeinen von Spinnen mit unterschiedlicher Lebensweise. Zool Beitr N F 29:209–225Google Scholar
  73. Paydar S, Doan CA, Jacobs CA (1999) Neural mapping of direction and frequency in the cricket cercal sensory system. J Neurosci 19:1771–1781PubMedGoogle Scholar
  74. Reissland A, Görner P (1985) Trichobothria. In: Barth FG (ed) Neurobiology of arachnids. Springer, Heidelberg, pp 138–161Google Scholar
  75. Santer RD, Hebets EA (2008) Agonistic signals received by arthropod filiform hair allude to the prevalence of near-field sound communication. Proc R Soc B 275:363–368PubMedCrossRefGoogle Scholar
  76. Schaber CF, Gorb SN, Barth FG (2012) Force transformation in spider strain sensors: white light interferometry. J R Soc Interface 9(71):1254–1264PubMedCentralPubMedCrossRefGoogle Scholar
  77. Schilstra C, van Hateren JH (1999) Blowfly flight and optic. I. Thorax kinematics and flight dynamics. J Exp Biol 202:1481–1490PubMedGoogle Scholar
  78. Schmidt K, Gnatzy W (1971) Die Feinstruktur der Sinneshaare auf den Cerci von Gryllus Deg (Saltatoria, Gryllidae). II. Die Häutung der Faden- und Keulenhaare. Z Zellforsch 122:210–226PubMedCrossRefGoogle Scholar
  79. Schuh RT (1975) The structure, distribution, and taxonomic importance of trichobothria in the Miridae (Hemiptera). Am Mus Novit 2585:1–26Google Scholar
  80. 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
  81. 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
  82. Shimozawa T, Murakami J, Kumagai T (1998) Cricket wind receptor cell detects mechanical energy of the level of kT of thermal fluctuation. Abstract 112, International Society of Neuroethology Conference, San DiegoGoogle Scholar
  83. Shimozawa T, Murakami J, Kumagai T (2003) Cricket wind receptors: thermal noise for the highest sensitivity known. In: Barth FG, Humphrey JAC, Secomb TW (eds) Sensors and sensing in biology and engineering, Chap 10. Springer, Wien, New York, pp 145–157Google Scholar
  84. 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
  85. Suter RB (2003) Trichobothrial mediation of an aquatic escape response: directional jumps by the fishing spider, Dolomedes triton, foil frog attacks. J Insect Sci 3:19–25PubMedCentralPubMedCrossRefGoogle Scholar
  86. Tautz J (1977) Reception of medium vibration by thoracal hairs of caterpillars of Barathra brassicae L. (Lepidoptera, Noctuidae). I. Mechanical properties of the receptor hairs. J Comp Physiol 118:13–31CrossRefGoogle Scholar
  87. Tautz J (1979) Reception of particle oscillation in a medium: an unorthodox sensory capacity. Naturwissenschaften 66:452–461CrossRefGoogle Scholar
  88. Tautz J, Markl H (1978) Caterpillars detect flying wasps by hairs sensitive to medium vibration. Behav Ecol Sociobiol 4:101–110CrossRefGoogle Scholar
  89. Theiß J (1979) Mechanoreceptive bristles on the head of the blowfly: mechanics and electrophysiology of the macrochaetae. J Comp Physiol 132:55–68CrossRefGoogle Scholar
  90. Thurm U (1982) Biophysik der Mechanorezeption. In: Hoppe W, Lohmann W, Markl H, Ziegler H (eds) Biophysik, 2nd edn. Springer, Berlin Heidelberg, pp 691–696Google Scholar
  91. Triblehorn JD, Yager DD (2006) Wind generated by an attacking bat: anemometric measurements and detection by the praying mantis cercal system. J Exp Biol 209:1430–1440PubMedCrossRefGoogle Scholar
  92. Tropaea C, Bleckmann H (2012) Nature-inspired fluid mechanics. Springer, Heidelberg, 372 ppCrossRefGoogle Scholar
  93. Vachon M (1973) Etude des caractères utilisées pour classer les familles et les genres de scorpions (Arachnides). 1. La trichobothriotaxie en arachnologie. Sigles trichobothriaux et types de trichobothriotaxie chez les scorpions. Bull Mus Hist Nat 3 Ser 140:857–958Google Scholar
  94. Weygoldt P (1995) A whip spider that ate rolled oats, with observations on prey-capture behaviour in whip spiders. Newsl Br Arachnol Soc 74:6–8Google Scholar
  95. Weygoldt P (2000) Whip spiders (Chelicerata: Amblypygi): their biology, morphology and systematics. Apollo Books, StenstrupGoogle Scholar
  96. Weygoldt P, Paulus H (1979) Untersuchungen zur Morphologie, Taxonomie und Phylogenie der Chelicerata. I. Morphologische Untersuchungen. Z zool Systematik Evolutionsforschung 17:85–116CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of Neurobiology, Faculty of Life SciencesUniversity of ViennaViennaAustria

Personalised recommendations