Skip to main content
Log in

Arousal from Tonic Immobility by Vibration Stimulus

  • Original Research
  • Published:
Behavior Genetics Aims and scope Submit manuscript

Abstract

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.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Humphreys RK, Ruxton GD (2018) A review of thanatosis (death feigning) as an anti-predator behaviour. Behav Ecol Sociobiol 72:22. https://doi.org/10.1007/s00265-017-2436-8

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Matsumura K, Miyatake T (2015) Differences in attack avoidance and mating success between strains artificially selected for dispersal distance in Tribolium castaneum. PLoS ONE. https://doi.org/10.1371/journal.pone.0127042

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Book  Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

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

    Article  Google Scholar 

  • 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)

    Google Scholar 

Download references

Acknowledgements

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

Authors and Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Takahisa Miyatake.

Ethics declarations

Conflict of interest

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

Ethical approval

This study was not required to complete an ethical assessment prior to conducting our research.

Human and animal rights and informed consent

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Edited by Stephen Clark Maxson.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 15 kb)

Supplementary material 2 (DOCX 146 kb)

Supplementary material 3 (MP4 2794 kb)

Supplementary material 4 (MP4 2834 kb)

Supplementary material 5 (MP4 2735 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10519-019-09962-x

Keywords

Navigation