Advertisement

Behavior Genetics

, Volume 49, Issue 5, pp 478–483 | Cite as

Arousal from Tonic Immobility by Vibration Stimulus

  • Takahisa MiyatakeEmail author
  • Kentarou Matsumura
  • Ryota Kitayama
  • Keiichi Otsuki
  • Ji Yuhao
  • Ryusuke Fujisawa
  • Naohisa Nagaya
Original Research

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.

Keywords

Beetle Crossing experiment Death feigning Selection experiment Thanatosis Tribolium 

Notes

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 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.

Compliance with ethical standards

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.

Supplementary material

10519_2019_9962_MOESM1_ESM.xlsx (15 kb)
Supplementary material 1 (XLSX 15 kb)
10519_2019_9962_MOESM2_ESM.docx (146 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)

References

  1. Acheampong S, Mitchell BK (1997) Quiescence in the Colorado potato beetle, Leptinotarsa decemlineata. Entomol Exp Appl 82:83–89CrossRefGoogle Scholar
  2. Cassill DL, Vo K, Becker B (2008) Young fire ant workers feign death and survive aggressive neighbors. Naturwissenschaften 95:617–624CrossRefGoogle Scholar
  3. Gregory PT, Gregory LA (2006) Immobility and supination in garter snakes (Thamnophis elegans) following handling by human predators. J Comp Psychol 120:262–268CrossRefGoogle Scholar
  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 273:1631–1636CrossRefGoogle Scholar
  5. Hozumi N, Miyatake T (2005) Body-size dependent difference in deathfeigning behavior of adult Callosobruchus chinensis. J Insect Behav 18:557–566CrossRefGoogle Scholar
  6. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Khelifa R (2017) Faking death to avoid male coercion: extreme sexual conflict resolution in a dragonfly. Ecology 98:1724–1726CrossRefGoogle Scholar
  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 36:49–154CrossRefGoogle Scholar
  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.  https://doi.org/10.1371/journal.pone.0127042 CrossRefPubMedPubMedCentralGoogle Scholar
  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 36:161–168CrossRefGoogle Scholar
  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 34:97–105CrossRefGoogle Scholar
  12. Matsumura K, Fuchikawa T, Miyatake T (2017) Decoupling of behavioral trait correlation across life stages in two holometabolous insects. Behav Genet 47:459–467CrossRefGoogle Scholar
  13. Miyatake T (2001a) Diurnal periodicity of death-feigning in Cylas formicarius (Coleoptera: Brentidae). J Insect Behav 14:421–432CrossRefGoogle Scholar
  14. Miyatake T (2001b) Effects of starvation on death-feigning in adults of Cylas formicarius (Coleoptera: Brentidae). Ann Entomol Soc Am 94:612–616CrossRefGoogle Scholar
  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 271:2293–2296CrossRefGoogle Scholar
  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 75:113–121CrossRefGoogle Scholar
  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 33:83–88CrossRefGoogle Scholar
  18. Nakayama S, Miyatake T (2009) Positive genetic correlations between life-history traits and death-feigning behavior in adzuki bean beetle. Evol Ecol 23:711–722CrossRefGoogle Scholar
  19. Nakayama S, Miyatake T (2010a) A behavioral syndrome in the adzuki bean beetle: genetic correlation among death feigning, activity, and mating behavior. Ethology 116:108–112CrossRefGoogle Scholar
  20. Nakayama S, Miyatake T (2010b) Genetic trade-off between abilities to avoid attack and to mate: a cost of tonic immobility. Biol Lett 6:18–20CrossRefGoogle Scholar
  21. Nakayama S, Nishi Y, Miyatake T (2010) Genetic correlation between behavioural traits in relation to death-feigning behaviour. Popul Ecol 52:329–335CrossRefGoogle Scholar
  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 58:750–755CrossRefGoogle Scholar
  23. Nishi Y, Sasaki K, Miyatake T (2010) Biogenic amines, caffeine and tonic immobility in Tribolium castaneum. J Insect Physiol 56:622–628CrossRefGoogle Scholar
  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 274:555–560CrossRefGoogle Scholar
  25. Prohammer LA, Wade MJ (1981) Geographic and genetic variation in death-feigning behavior in the flour beetle, Tribolium castaneum. Behav Genet 11:395–401CrossRefGoogle Scholar
  26. Rogers SM, Simpson SJ (2014) Thanatosis. Curr Biol 24:R1031–R1033CrossRefGoogle Scholar
  27. Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack. Oxford University Press, OxfordCrossRefGoogle Scholar
  28. SAS Institute Inc (2015) JMP 12.2.0. SAS Institute Inc., CaryGoogle Scholar
  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 29:170–178Google Scholar
  30. Skelhorn J (2018) Avoiding death by feigning death. Curr Biol 28:R1121–R1142CrossRefGoogle Scholar
  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) Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Evolutionary Ecology, Graduate School of Environmental and Life ScienceOkayama UniversityOkayamaJapan
  2. 2.Faculty of Computer Science and EngineeringKyoto Sangyo UniversityKyotoJapan
  3. 3.School of Computer Science and Systems EngineeringKyushu Institute of TechnologyIizuka-shiJapan

Personalised recommendations