Arousal from Tonic Immobility by Vibration Stimulus


Tonic immobility (TI) is an effective anti-predator strategy. However, long immobility status on the ground increases the risk of being eaten by predators, and thus insects must rouse themselves when appropriate stimulation is provided. Here, the strength of vibration causing arousal from the state of TI was examined in strains artificially selected for longer duration of TI (L-strains: long sleeper) in a beetle. We provided different strengths of vibration stimuli to the long sleepers in Tribolium castaneum. Although immobilized beetles were never awakened by the stimuli from 0.01 to 0.12 mm in amplitude, almost of the beetles were aroused from immobilized status by the stimulus at 0.21 mm. There was a difference in sensitivity of individuals when the stimuli of 0.14 mm and 0.18 mm were provided. F2 individuals were also bred by crossing experiments of the strains selected for shorter and longer duration of TI. The arousal sensitivity to vibration was well separated in the F2 individuals. A positive relationship was observed between the duration of TI and the vibration amplitude, suggesting that immobilized beetles are difficult to arouse from a deep sleep, while light sleepers are easily aroused by even small vibrations. The results indicate a genetic basis for sensitivity to arousal from TI.

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  1. Acheampong S, Mitchell BK (1997) Quiescence in the Colorado potato beetle, Leptinotarsa decemlineata. Entomol Exp Appl 82:83–89

  2. Cassill DL, Vo K, Becker B (2008) Young fire ant workers feign death and survive aggressive neighbors. Naturwissenschaften 95:617–624

  3. Gregory PT, Gregory LA (2006) Immobility and supination in garter snakes (Thamnophis elegans) following handling by human predators. J Comp Psychol 120:262–268

  4. Honma A, Oku S, Nishida T (2006) Adaptive significance of death feigning posture as a specialized inducible defence against gape-limited predators. Proc R Soc B 273:1631–1636

  5. Hozumi N, Miyatake T (2005) Body-size dependent difference in deathfeigning behavior of adult Callosobruchus chinensis. J Insect Behav 18:557–566

  6. Humphreys RK, Ruxton GD (2018) A review of thanatosis (death feigning) as an anti-predator behaviour. Behav Ecol Sociobiol 72:22.

  7. Khelifa R (2017) Faking death to avoid male coercion: extreme sexual conflict resolution in a dragonfly. Ecology 98:1724–1726

  8. Kuriwada T, Kumano N, Shiromoto K, Haraguchi D (2011) Age-dependent investment in death-feigning behaviour in the sweetpotato weevil Cylas formicarius. Physiol Entomol 36:49–154

  9. Matsumura K, Miyatake T (2015) Differences in attack avoidance and mating success between strains artificially selected for dispersal distance in Tribolium castaneum. PLoS ONE.

  10. Matsumura K, Miyatake T (2018) Responses to relaxed and reverse selection in strains artificially selected for duration of death-feigning behavior in the red flour beetle, Tribolium castaneum. J Ethol 36:161–168

  11. Matsumura K, Sasaki K, Miyatake T (2016) Correlated responses in death-feigning behavior, activity, and brain biogenic amine expression in red flour beetle Tribolium castaneum strains selected for walking distance. J Ethol 34:97–105

  12. Matsumura K, Fuchikawa T, Miyatake T (2017) Decoupling of behavioral trait correlation across life stages in two holometabolous insects. Behav Genet 47:459–467

  13. Miyatake T (2001a) Diurnal periodicity of death-feigning in Cylas formicarius (Coleoptera: Brentidae). J Insect Behav 14:421–432

  14. Miyatake T (2001b) Effects of starvation on death-feigning in adults of Cylas formicarius (Coleoptera: Brentidae). Ann Entomol Soc Am 94:612–616

  15. Miyatake T, Katayama K, Takeda Y, Nakashima A, Sugita A, Mizumoto M (2004) Is death-feigning adaptive? Heritable variation in fitness difference of death-feigning behaviour. Proc R Soc Lond B 271:2293–2296

  16. Miyatake T, Tabuchi K, Sasaki K, Okada K, Katayama K, Moriya S (2008a) Pleiotropic antipredator strategies, fleeing and feigning death, correlated with dopamine levels in Tribolium castaneum. Anim Behav 75:113–121

  17. Miyatake T, Okada K, Harano T (2008b) Negative relationship between ambient temperature and death-feigning intensity in adult Callosobruchus maculatus and Callosobruchus chinensis. Physiol Entomol 33:83–88

  18. Nakayama S, Miyatake T (2009) Positive genetic correlations between life-history traits and death-feigning behavior in adzuki bean beetle. Evol Ecol 23:711–722

  19. Nakayama S, Miyatake T (2010a) A behavioral syndrome in the adzuki bean beetle: genetic correlation among death feigning, activity, and mating behavior. Ethology 116:108–112

  20. Nakayama S, Miyatake T (2010b) Genetic trade-off between abilities to avoid attack and to mate: a cost of tonic immobility. Biol Lett 6:18–20

  21. Nakayama S, Nishi Y, Miyatake T (2010) Genetic correlation between behavioural traits in relation to death-feigning behaviour. Popul Ecol 52:329–335

  22. Nakayama S, Sasaki K, Matsumura K, Lewis Z, Miyatake T (2012) Dopaminergic system as the mechanism underlying personality in a beetle. J Insect Physiol 58:750–755

  23. Nishi Y, Sasaki K, Miyatake T (2010) Biogenic amines, caffeine and tonic immobility in Tribolium castaneum. J Insect Physiol 56:622–628

  24. Ohno T, Miyatake T (2007) Drop or fly? Negative genetic correlation between death-feigning intensity and flying ability as alternative anti-predator strategies. Proc R Soc B 274:555–560

  25. Prohammer LA, Wade MJ (1981) Geographic and genetic variation in death-feigning behavior in the flour beetle, Tribolium castaneum. Behav Genet 11:395–401

  26. Rogers SM, Simpson SJ (2014) Thanatosis. Curr Biol 24:R1031–R1033

  27. Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack. Oxford University Press, Oxford

  28. SAS Institute Inc (2015) JMP 12.2.0. SAS Institute Inc., Cary

  29. Shaheen FA, Parveen S, Zia A, Qadir G, Husain M, Khan RU (2016) Predatory aptness of ants against red flour beetle, Tribolium castaneum Herbst (Tenebrionidae: Coleoptera) in wheat flour. Pak J Agric Res 29:170–178

  30. Skelhorn J (2018) Avoiding death by feigning death. Curr Biol 28:R1121–R1142

  31. Suzuki T, Nakakita H (1991) Tribolium castaneum (HERBEST), T. confusum J. du V., T. freemani Hinton. In: Yushima K, Kamano S, Tamaki Y (eds) Rearing methods of insects. Nihon Shokubutsu-Boueki Kyokai, Tokyo, pp 251–254 (In Japanese)

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We thank Mrs. N Hayashi for assistance of the experiment. This work was supported by a Grant from Grant-in-Aid for Scientific Research, KAKENHI 17H05976 and 18H02510, MEXT, JSPS to T.M.

Author information

T.M. designed the study. K.M., R.K., K.O., J.Y. T.M. collected data. T.M., KM analysed the data. TM, RF, NN interpreted the results and wrote the manuscript. All authors gave final approval for publication.

Correspondence to Takahisa Miyatake.

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Takahisa Miyatake, Kentarou Matsumura, Ryota Kitayama, Keiichi Otsuki, Ji Yuhao, Ryusuke Fujisawa and Naohisa Nagaya declare that they have no conflict of interest.

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Miyatake, T., Matsumura, K., Kitayama, R. et al. Arousal from Tonic Immobility by Vibration Stimulus. Behav Genet 49, 478–483 (2019) doi:10.1007/s10519-019-09962-x

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  • Beetle
  • Crossing experiment
  • Death feigning
  • Selection experiment
  • Thanatosis
  • Tribolium