Morpho-Functional Characterization of Cercal Organs in Crickets

Abstract

The involvement of the cercal organs in triggering of motor responses to acoustic stimulation was comparatively investigated in a cricket Phaeophelacris bredoides imago, which lost the tympanal organ during evolution, and a cricket Gryllus bimaculatus last-instar nymph that has a rudimentary tympanal organ. A morphometric analysis of the cercal filiform sensilla in both species revealed that in Ph. bredoides a single cercus bears mainly longer hairs (total number, 1110 ± 16) that vary in their length from 800 to 1850 µm, while in G. bimaculatus nymphs the filiform sensilla on a single cercus are fewer (total number, 845 ± 27) and predominantly shorter (<200 µm). The frequency range of signals triggering motor responses in Ph. bredoides imagines shifts towards higher frequencies, while in G. bimaculatus nymphs it expands with the increasing sound intensity. The data obtained indicate that, while triggering motor responses, the cercal organ in Ph. bredoides is functionally complemented by other mechanosensory organs. In G. bimaculatus, sensillar responses of the nymphal cercal organ are required for initiating motor responses but are not compensated by other organs at physiological sound intensities.

This is a preview of subscription content, access via your institution.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

REFERENCES

  1. 1

    Alexander, R.D., Aggressiveness, territoriality, and sexual behavior in field crickets (Orthoptera: Gryllidae), Behav., 1961, vol. 17(23), pp. 130–223. https://www.jstor.org/stable/4532972

  2. 2

    Ronacher, B., Hennig, R.M., and Clemens, J., Computational principles underlying recognition of acoustic signals in grasshoppers and crickets, J. Comp. Physiol. A, 2015, vol. 201(1), pp. 61–71. doi: 10.1007/BF00605455

  3. 3

    Horch, H.W., Mito, T., Popadic, A., Ohuchi, H., and Noji, S., The Cricket as a Model Organism, Horch, H.W., Mito, T., Popadić, A., Ohuchi, H., and Noji, S., Eds., Springer, Tokyo, 2017. doi: 10.1007/978-4-431-56478-2

  4. 4

    Hoy, R.R. and Robert, D., Tympanal hearing in insects, Annu. Rev. Entomol., 1996, vol. 41(1), pp. 433–450. doi: 10.1146/annurev.en.41.010196.002245

  5. 5

    Strauß, J. and Stumpner, A., Selective forces on origin, adaptation and reduction of tympanal ears in insects, J. Comp. Physiol. A, 2015, vol. 201(1), pp. 155–169. doi: 10.1007/s00359-014-0962-7

  6. 6

    Shimozawa, T., Kumagai, T., and Baba, Y., Structural scaling and functional design of the cercal wind-receptor hairs of cricket, J. Comp. Physiol. A, 1998, vol. 183(2), pp. 171–186. doi: 10.1007/s003590050245

  7. 7

    Magal, C., Dangles, O., Caparroy, P., and Casas, J., Hair canopy of cricket sensory system tuned to predator signals, J. Theor. Biol., 2006, vol. 241(3), pp. 459–466. doi: 10.1016/j.jtbi.2005.12.009

  8. 8

    Dambach, M. and Huber, F., Perception of substrate-vibration in crickets, Symp. Mechanoreception, VS Verlag für Sozialwissenschaften, 1974, Wiesbaden, pp. 263–280. doi: 10.1007/978-3-663-01719-6_19

  9. 9

    Yack, J.E., The structure and function of auditory chordotonal organs in insects, Microsc. Res. Tech., 2004, vol. 63(4), pp. 315–337. doi: 10.1002/jemt.20051

  10. 10

    Kleindienst, H.U., Wohlers, D.W., and Larsen, O.N., Tympanal membrane motion is necessary for hearing in crickets, J. Comp. Physiol. A, 1983, vol. 151(4), pp. 397–400. doi: 10.1007/BF00605455

  11. 11

    Lankheet, M.J., Cerkvenik, U., Larsen, O.N., and Leeuwen, J.L., Frequency tuning and directional sensitivity of tympanal vibrations in the field cricket Gryllus bimaculatus, J. Royal. Soc. Interface, 2017, vol. 14(128). doi: 10.1098/rsif.2017.0035

  12. 12

    Fukutomi, M. and Ogawa, H., Crickets alter wind-elicited escape strategies depending on acoustic context, Sci. Rep., 2017, vol. 7(1), pp. 1–8. doi: 10.1038/s41598-017-15276-x

  13. 13

    Loher, W. and Dambach, M., Reproductive behavior, Cricket Behavior and Neurobiology, Huber, F., Moore, T., and Loher, W., Eds., Ithaca, New York, 1989, pp. 43–82.

  14. 14

    Cokl, A. and Virant-Doberlet, M., Vibrational communication, Encyclopedia of Insects, Resh, V.H. and Carde, R.T., Eds., Amsterdam, 2009, pp. 1034–1038. doi: 10.1590/S1519-566X2004000200001

  15. 15

    Eibl, E., Morphology of the sense organs in the proximal parts of the tibiae of Gryllus campestris L. and Gryllus bimaculatus deGeer (Insecta, Ensifera), Zoomorphol., 1978, vol. 89(3), pp. 185–205. doi: 10.1007/BF00993947

  16. 16

    Shimozawa, T. and Kanou, M., Varieties of filiform hairs: range fractionation by sensory afferents and cercal interneurons of a cricket, J. Comp. Physiol. A, 1984, vol. 155(4), pp. 485–493. doi: 10.1007/BF00611913

  17. 17

    Knyazev, A.N., A study of the influence of various mechanosensory systems of the cricket Gryllus bimaculatus De Geer on triggering of motor reactions, Zh. Evol. Biokhim. Fiziol., 1986, vol. 22(3), pp. 284–293.

  18. 18

    Rozhkova, G.I., Vedenina, V.Y., and Kamper, G., Frequency-intensity characteristics of cricket cercal interneurons: broadband units, J. Comp. Physiol. A, 1999, vol. 184, pp. 161–167. doi: 10.1007/s003590050315

  19. 19

    Hoy, R., Nolen, T., and Brodfuehrer, P., The neuroethology of acoustic startle and escape in flying insects, J. Exp. Biol., 1989, vol. 146(1), pp. 287–306. https://jeb.biologists.org/content/146/1/287.short

  20. 20

    Čokl, A., Kalmring, K., and Rössler, W., Physiology of atympanate tibial organs in forelegs and midlegs of the cave-living Ensifera, Troglophilus neglectus (Rhaphidophoridae, Gryllacridoidea), J. Exp. Zool., 1995, vol. 273, pp. 376–388. doi: 10.1002/jez.1402730503

  21. 21

    Peljhan, N.S. and Strauß, J., The mechanical leg response to vibration stimuli in cave crickets and implications for vibrosensory organ functions, J. Comp. Physiol A, 2018, vol. 204(7), pp. 687–702. doi: 10.1007/s00359-018-1271-3

  22. 22

    Knyazev, A.N., Interaction of mechanoreceptor systems as a basic for acoustic communication in insect, Sensory Systems and Communication in Arthropods, Birkhauser Verlag Basel, 1990, pp. 265–270. doi: 10.1007/978-3-0348-6410-7_45

  23. 23

    Fukutomi, M., Someya, M., and Ogawa, H., Auditory modulation of wind-elicited walking behavior in the cricket Gryllus bimaculatus, J. Exp. Biol., 2015, vol. 218(24), pp. 3968–3977. doi: 10.1242/jeb.128751

  24. 24

    Ball, E. and Young, D., Structure and development of the auditory system in the prothoracic leg of the cricket Teleogryllus commodus (Walker), II. Postembryonic development, Cell. Tissue. Res., 1974, vol. 147(3), pp. 313–324. doi: 10.1007/BF00307467

  25. 25

    Klose, M., Development of leg chordotonal sensory organs in normal and heat shocked embryos of the cricket Teleogryllus commodus (Walker), Roux’s. Arch. Dev. Biol., 1996, vol. 205(7–8), pp. 344–355. doi: 10.1007/BF00377214

  26. 26

    Nishino, H., Domae, M., Takanashi, T., and Okajima, T., Cricket tympanal organ revisited: morphology, development and possible functions of the adult-specific chitin core beneath the anterior tympanal membrane, Cell Tiss. Res., 2019, vol. 377(2), pp. 193–214. doi: 10.1007/s00441-019-03000-2

  27. 27

    Desutter-Grandcolas, L., Toward the knowledge of the evolutionary biology of phalangopsid crickets (Orthoptera: Grylloidea: Phalangopsidae). Data, questions and evolutionary scenarios, J. Orth. Res., 1996, vol. 4, pp. 163–175. doi: 10.2307/3503472

  28. 28

    Heidelbach, J. and Dambach, M., Wing-flick signals in the courtship of the african cave cricket, Phaeophilacris spectrum, Ethology, 1997, vol. 103(10), pp. 827–843. doi: 10.1111/j.1439-0310.1997.tb00124.x

  29. 29

    Gorochov, A.V., New and little known Phalangopsinae (Orthoptera, Gryllidae), 9. The African genus Phaeophilacris, Entomol. Rev., 2015, vol. 95(8), pp. 1112–1124. doi: 10.1134/S0013873812010071

  30. 30

    Lunichkin, A.M., Zhemchuzhnikov, M.K., and Knyazev, A.N., Basic elements of behavior of the cricket Phaeophilacris bredoides Kaltenbach (Orthoptera, Gryllidae), Entomol. Rev., 2016, vol. 96(5), pp. 537–544. doi: 10.1134/S0013873816050031

  31. 31

    Shimozawa, T., Murakami, J., and Kumagai, T., Cricket wind receptors: thermal noise for the highest sensitivity known, Sensors and Sensing in Biology and Engineering. Springer, Barth, F.G., Humphrey, J.A.C., and Secomb, T.W., Eds., Vienna, 2003, pp. 145–157. doi: 10.1007/978-3-7091-6025-1_10

  32. 32

    Miller, J.P., Krueger, S., Heys, J.J., and Gedeon, T., Quantitative characterization of the filiform mechanosensory hair array on the cricket cercus, PloS One, 2011, vol. 6(11). doi: 10.1371/journal.pone.0027873

  33. 33

    Cummins, B., Gedeon, T., Klapper, I., and Cortez, R., Interaction between arthropod filiform hairs in a fluid environment, J. Theor. Biol., 2007, vol. 247(2), pp. 266–280. doi: 10.1016/j.jtbi.2007.02.003

  34. 34

    Knyazev, A.N. and Popov, A.V., Response of single cercal mechanoreceptors of cricket to sound and sinusoidal mechanical stimulation, Dokl. Akad. Nauk SSSR, 1977, vol. 232, pp. 1211–1214.

  35. 35

    Lunichkin, A.M. and Knyazev, A.N., Involvement of the mechanosensory complex structures of the cricket Phaeophilacris bredoides in triggering of motor responses to sound, J. Evol. Biochem. Physiol., 2017, vol. 53(6), pp. 480–492. doi: 10.1134/S0022093017060059

  36. 36

    Lunichkin, A.M. and Knyazev, A.N., Involvement of mechanosensory complex structures of the cricket Gryllus bimaculatus larvae (Orthoptera, Gryllidae) in triggering of motor responses to sound, J. Evol. Biochem. Physiol., 2018, vol. 54(2), pp. 137–148. doi: 10.1134/S0022093018020072

  37. 37

    Lunichkin, A.M., Zhemchuzhnikov, M.K., and Knyazev, A.N., Ontogeny of the cricket Phaeophilacris bredoides Kaltenbach (Orthoptera, Gryllidae), Entomol. Rev., 2013, vol. 93(1), pp. 19–29. doi: 10.1134/S0013873813010041

  38. 38

    Knyazev, A.N. and Chudakova, I.V., Effect of allatectomy on phonotaxis in the cricket Gryllus bimaculatus De Geer, J. Evol. Biochem. Physiol., 1990, vol. 26(6), pp. 695–701.

  39. 39

    Knyazev, A.N., Ivanov, V.P., and Vorobyeva, O.N., Interaction of distant mechanoreceptor systems under conditions of presentation of non-specific sound signals to normal and allatectomized female crickets Gryllus bimaculatus, J. Evol. Biochem. Physiol., 1999, vol. 35(6), pp. 289–294. doi: 10.1023/A:1017535007233

  40. 40

    Knyazev, A.N., Ivanov, V.P., and Vorobyeva, O.N., Interaction of distant mechanoreceptor systems under conditions of presentation of conspecific sound signals to normal and allatectomized male crickets Gryllus bimaculatus, J. Evol. Biochem. Physiol., 2000, vol. 36(6), pp. 760–766. doi: 10.1023/A:1017535007233

  41. 41

    Zhemchuzhnikov, M.K. and Knyazev, A.N., Development of sexual and protective behavior of female crickets Gryllus argentinus Sauss. at the prereproductive and reproductive periods of imaginal ontogenesis, J. Evol. Biochem. Physiol., 2011, vol. 47(6), pp. 565–570. doi: 10.1134/S0022093011060081

  42. 42

    Lunichkin, A.M., Baulin, Y.A., Zhukovskaya, M.I., and Knyazev, A.N., Evaluation of the method of inactivation of cricket cercal sensilla using electrocercogram, Sens. Sist., 2019, vol. 33(4), pp. 351–354.

  43. 43

    Heidelbach, J., Dambach, M., and Böhm, H., Processing wing flick-generated air-vortex signals in the african cave cricket, Phaeophilacris spectrum, Naturwiss., 1991, vol. 78(6), pp. 277–278.

  44. 44

    Altman, Y.A., Vartanyan, I.A., Gorlinskiy, I.A., Bigday, E.V., Samoylov, V.O., Nosdrachev, A.D., and Alekseev, N.P., Fiziologiya sensornykh system i vysshei nervnoi deyatel’nosti, Tom 1, Fiziologiya Sensornykh Sistem (Physiology of sensory systems and higher nervous activity, vol. 1, Physiology of Sensory Systems), St. Petersburg, 2009.

  45. 45

    Slinker, K., Kondash, C., Dickinson, B.T., and Baur, J.W., High-bandwidth and sensitive air flow sensing based on resonance properties of CNT-on-fiber hairs, J. Carbon. Res., 2017, vol. 3(1), p. 6. doi: 10.3390/c3010006

  46. 46

    Roddey, J.C. and Jacobs, G.A., Information theoretic analysis of dynamical encoding by filiform mechanoreceptors in the cricket cercal system, J. Neurophysiol., 1996, vol. 75(4), pp. 1365–1376. doi: 10.1152/jn.1996.75.4.1365

Download references

ACKNOWLEDGMENTS

Authors are grateful to B.F. Gribakin (St. Petersburg State University) for his help in interpreting cave cricket’s cercal responses to high-frequency stimuli at a highest intensity of sound stimulation.

Funding

This work was supported by the State budget (theme reg. no. АААА-А18-118013090245-6).

Author information

Affiliations

Authors

Contributions

A.M. Lunichkin—experimental design, data collection and processing, writing and editing a manuscript; M.I. Zhukovskaya—data processing, writing and editing a manuscript.

Corresponding author

Correspondence to A. M. Lunichkin.

Ethics declarations

All applicable international, national and institutional principles of handling and using experimental animals for scientific purposes were observed. This study did not involve human subjects as research objects.

Additional information

Translated by A. Polyanovsky

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lunichkin, A.M., Zhukovskaya, M.I. Morpho-Functional Characterization of Cercal Organs in Crickets. J Evol Biochem Phys 57, 46–54 (2020). https://doi.org/10.1134/S002209302101004X

Download citation

Keywords:

  • evolution
  • ontogeny
  • sensory systems
  • bioacoustics
  • insects
  • crickets