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Journal of Comparative Physiology A

, Volume 155, Issue 6, pp 725–738 | Cite as

Auditory behavior of the cricket

III. Tracking of male calling song by surgically and developmentally one-eared females, and the curious role of the anterior tympanum
  • Franz Huber
  • H. -U. Kleindienst
  • Theo Weber
  • John Thorson
Article

Summary

  1. 1.

    Many one-eared female crickets (Gryllus campestris andGryllus bimaculatus), whether the loss is due to surgery or to developmental accident, can maintain characteristic, stable courses with respect to the direction of male calling song, when tested on the Kramer spherical tread-mill. The error angles are usually less than 90°, so that Regen's (1924) remark about the success of such females in finding singing males is supported.

     
  2. 2.

    Some females with developmental unilateral hearing deficit, confirmed both histologically and by sparing of tracking after removal of the suspect leg, track nearly as accurately as normal animals with two ears.

     
  3. 3.

    Experiments in which tympana were immobilized with wax, whether tracking behavior or interneuron responses were monitored, show that the anterior tympanum — considered for some time to be irrelevant to hearing — mediates appreciable sound input to the auditory receptors, at least when the posterior tympana are blocked.

     
  4. 4.

    The above results resolve two current paradoxes regarding comparison of tympanum immobilization in behavior with the mechanics of receptor excitation:

    First, because even unambiguously one-eared animals can maintain stable sound-oriented courses, such tracking performance with waxed tympana does not argue that total tympanal immobilization spares some auditory function of that ear (cf. Schmitz et al. 1983). The argument assumes that tracking would not be expected if one ear were silenced; the assumption is evidently false.

    Second, it has been unclear why waxing of both posterior tympana raises tracking threshold only ca. 20 dB (Schmitz 1983) whereas the tympanalmechanics studies of Kleindienst et al. (1983) have suggested a much greater deficit. Our finding that one must wax the anterior tympana as well, in order to produce deficit greater than ca. 20 dB, clarifies the situation. That is, in the biophysical experiments both tympana of the leg were immobilized by the procedures used (pressure matching and water immersion), whereas in most current behavioral tympanum-waxing experiments (but not in those of Bailey and Thomson 1977) the anterior tympana have been ignored.

     
  5. 5.

    A novel behavioral effect was observed with all four tympana blocked. Thresholds for orientation were ca. 90–100 dB, but in every case the animals tended to walk away from the loudspeaker.

     
  6. 6.

    The search for an explanation of one-eared tracking leads us to analogies with the recovery from imbalance following such surgery as hemilabyrinthectomy in vertebrates. A ‘phantom tympanum’, on the side with deficit, could in principle participate in corrective tracking, by the usual notions of bilateral comparison.

     

Keywords

Error Angle Male Calling Calling Song Walk Away Bilateral Comparison 
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.

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References

  1. Bailey WJ, Thomson P (1977) Acoustic orientation in the cricketTeleogryllus oceanicus (Le Guillou). J Exp Biol 67:61–75Google Scholar
  2. Ball EE (1979) Development of the auditory tympana in the cricketTeleogryllus commodus (Walker): Experiments on regeneration and transplantation. Experientia 35:324–325Google Scholar
  3. Ball EE, Cowan AN (1978) Ultrastructural study of the development of the auditory tympana in the cricketTeleogryllus commodus (Walker). J Embryol Exp Morphol 46:75–87Google Scholar
  4. Ball EE, Young D (1974) Structure and development of the auditory system in the prothoracic leg of the cricketTeleogryllus commodus (Walker). II. Postembryonic development. Z Zellforsch 147:313–324Google Scholar
  5. Biggin RJ (1981) Pattern re-establishment — transplantation and regeneration of the leg in the cricketTeleogryllus commodus (Walker). J Embryol Exp Morphol 61:87–101Google Scholar
  6. Boyd P, Lewis B (1983) Peripheral auditory directionality in the cricket (Gryllus campestris L.,Teleogryllus oceanicus Le Guillou). J Comp Physiol 153:523–532Google Scholar
  7. Fletcher NH, Thwaites S (1979) Acoustical analysis of the auditory system of the cricketTeleogryllus commodus (Walker). J Acoust Soc Am 66:350–357Google Scholar
  8. Flohr H, Precht W (1981) Lesion-induced neuronal plasticity in sensorimotor systems. Springer, Berlin Heidelberg NewYorkGoogle Scholar
  9. Fraenkel GS, Gunn DL (1961) The orientation of animals, (reprinted) Dover, New YorkGoogle Scholar
  10. Harris J, Ghiradella H (1980) The forces exerted on the substrate by walking and stationary crickets. J Exp Biol 85:263–279Google Scholar
  11. Holst E von (1950) Die Arbeitsweise des Statolithenapparates bei Fischen. Z Vergl Physiol 32:60–120Google Scholar
  12. Huber F (1983) Der Weg vom Verhalten zur einzelnen Nervenzelle. Studien an Grillen. Akad Wiss Lit Mainz (Jahrgang 1982, Nr. 3) Steiner, WiesbadenGoogle Scholar
  13. Johnstone BM, Saunders JC, Johnstone JR (1970) Tympanic membrane response in the cricket. Nature 227:625–626Google Scholar
  14. Kleindienst H-U, Wohlers DW, Larsen ON (1983) Tympanal membrane motion is necessary for hearing in crickets. J Comp Physiol 151:397–400Google Scholar
  15. Klopffleisch K-D (1973) Ethologische Untersuchungen an der FeldgrilleGryllus campestris L., an natürlichen Standorten. Examensarbeit Biologie, Universität KölnGoogle Scholar
  16. Kramer E (1975) Orientation of the male silkmoth to the sex attractant bombykol. In: Denton D, Coghlan JD (eds) Olfaction and taste, vol 5. Academic Press, New York, pp 329–335Google Scholar
  17. Kramer E (1976) The orientation of walking honeybees in odour fields with small concentration gradients. Physiol Entomol 1:27–37Google Scholar
  18. Kühne R, Silver S, Lewis B (1983) Processing of vibratory and acoustic signals by ventral cord neurons in the cricketGryllus campestris. J Insect Physiol 30:575–585Google Scholar
  19. Larsen ON, Michelsen A (1978) Biophysics of the ensiferan ear. III. The cricket ear as a four-input system. J Comp Physiol 123:217–227Google Scholar
  20. Lubbock J (1888) The senses, instincts and intelligence of animals, with special reference to insects. Kegan Paul Trench & Co, LondonGoogle Scholar
  21. Michel K (1974) Das Tympanalorgan vonGryllus bimaculatus DeGeer (Saltatoria, Gryllidae). Z Morphol Tiere 77:285–315Google Scholar
  22. Mörchen A, Rheinlaender J, Schwartzkopff J (1978) Latency shift in insect auditory nerve fibers. Naturwissenschaften 65:656–657Google Scholar
  23. Murphey RK, Zaretsky MD (1972) Orientation to calling song by female crickets,Scapsipedus marginatus (Gryllidae). J Exp Biol 56:335–352Google Scholar
  24. Paton JA, Capranica RR, Dragsten PR, Webb WW (1977) Physical basis for auditory frequency analyis in field crickets (Gryllidae). J Comp Physiol 119:221–240Google Scholar
  25. Pollack GS, Huber F, Weber T (1984) Frequency and temporal pattern dependent phonotaxis of crickets (Teleogryllus oceanicus) during tethered flight and compensated walking. J Comp Physiol A 154:13–26Google Scholar
  26. Popov AV, Shuvalov VF (1977) Phonotactic behavior of crickets. J Comp Physiol 119:111–126Google Scholar
  27. Precht W (1978) Neuronal operations in the vestibular system. Springer, Berlin Heidelberg New YorkGoogle Scholar
  28. Precht W (1983) The role of multisensory convergence in functional recovery after neural lesions. In: Horn E (ed) Multi-modal convergences in sensory systems. Fischer, Stuttgart, p 275Google Scholar
  29. Regen J (1924; sometimes cited as 1923, when his lecture was given Über die Orientierung des Weibchens vonLiogryllus campestris L. nach dem Stridulationsschall des Männchens. Ein Beitrag zur Physiologie des tympanalen Sinnesorgans. Akad Wiss Wien Math Nat Klasse Abt I 132:81–88Google Scholar
  30. Regen J (1926) Über die Beeinflussung der Stridulation vonThamnotrizon apterus Fab. ♂ durch künstlich erzeugte Töne und verschiedenartige Geräusche. Akad Wiss Wien Math Nat Klasse Abt. I 135:329–368Google Scholar
  31. Schildberger K (1984) Temporal selectivity of identified auditory neurons in the cricket brain. J Comp Physiol A 155:171–185Google Scholar
  32. Schmitz B (1983) Analyse der akustischen Orientierung bei Grillenweibchen (Gryllus campestris L.). Dissertation, KölnGoogle Scholar
  33. Schmitz B, Scharstein H, Wendler G (1983) Phonotaxis inGryllus campestris L. II. Acoustic orientation of female crickets after occlusion of single sound entrances. J Comp Physiol 152:257–264Google Scholar
  34. Schoen L (1950) Quantitative Untersuchungen über die zentrale Kompensation nach einseitiger Utriculusausschaltung bei Fischen. Z Vergl Physiol 32:121–150Google Scholar
  35. Schöne H (1980) Orientierung im Raum. Formen und Mechanismen der Lenkung des Verhaltens im Raum bei Tier und Mensch. Wissenschaftliche Verlagsgesellschaft, Stuttgart, p 257, Fig. 3.6/20Google Scholar
  36. Thorson J, Weber T, Huber F (1982) Auditory behavior of the cricket. II. Simplicity of calling-song recognition inGryllus, and anomalous phonotaxis at abnormal carrier frequencies. J Comp Physiol 146:361–378Google Scholar
  37. Weber T (1978) Vergleich der Lockgesänge von drei Grillenarten im Hinblick auf artspezifisches Erkennen in der Phonotaxis der Weibchen. Verh Dtsch Zool Ges 1978:176Google Scholar
  38. Weber T, Thorson J, Huber F (1981) Auditory behavior of the cricket. I. Dynamics of compensated walking and discrimination paradigms on the Kramer treadmill. J Comp Physiol 141:215–232Google Scholar
  39. Wendler G (1975) Physiology and systems analysis of gravity orientation in two insect species (Carausius morosus, Calandra granaria). Fortschr Zool 23:33–48Google Scholar
  40. Wendler G, Dambach M, Schmitz B, Scharstein H (1980) Analysis of the acoustic orientation behavior in crickets (Gryllus campestris L.). Naturwissenschaften 67:99–101Google Scholar
  41. Wohlers DW, Huber F (1982) Processing of sound signals by six types of neurons in the prothoracic ganglion of the cricket,Gryllus campestris L. J Comp Physiol 146: 161–173Google Scholar
  42. Zaretsky MD (1972) Specificity of the calling song and short term changes in the phonotactic response by female cricketsScapsipedus marginatus (Gryllidae). J Comp Physiol 79:153–172Google Scholar
  43. Zhantiev RD, Kalinkina IN, Chukanov VS (1975) Characteristics of the directional sensitivity of the tympanal organs in the cricketGryllus bimaculatus Deg. (Orthoptera, Gryllidae). Entomol Obozr 54:249–257Google Scholar

Copyright information

© Springer-Verlag 1984

Authors and Affiliations

  • Franz Huber
    • 1
  • H. -U. Kleindienst
    • 1
  • Theo Weber
    • 1
  • John Thorson
    • 1
  1. 1.Abteilung Huber, Max-Planck-Institut für VerhaltensphysiologieSeewiesenFederal Republic of Germany

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