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Behavioural interference among eusocial naked mole rats during work

Journal of Ethology volume 37, pages 101–109 (2019)Cite this article

Abstract

It has been reported that individuals of cooperative breeding species occasionally interfere with the work of other group members. However, the occurrence and function of this behaviour are controversial. In the naked mole rat (Heterocephalus glaber), a eusocial mammal, individuals frequently perform ‘tail-tugging’ behaviour, in which an actor holds the tail of another individual with the mouth and pulls that individual to a different place. In this study, we investigated the possible function of this behaviour in the experimental setting of soil excavation. Behavioural observations on three colonies showed that this behaviour was performed and received by individuals of all individual categories (i.e. queen, reproductive males, and workers), although a queen in one colony performed 72.5% of the observed behaviour. Our data support the hypothesis that this behaviour is used to monopolise work in a specific space because (1) tail-tugging was more likely to occur when the actor and recipient were working than when they were not, and (2) the actor performed tail-tugging in a cell in which that individual worked frequently. This study provides a rare example of behavioural interference in a cooperative society and suggests that there is disagreement and conflict regards the opportunity to work among colony members in this eusocial mammal.

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References

  • Bennett NC, Faulkes CG (2000) African mole-rats: ecology and eusociality. Cambridge University Press, Cambridge, p 273

    Google Scholar 

  • Bergmüller R, Johnstone RA, Russell AF, Bshary R (2007a) Integrating cooperative breeding into theoretical concepts of cooperation. Behav Proc 76:61–72

    Article  Google Scholar 

  • Bergmüller R, Russell AF, Johnstone RA, Bshary R (2007b) On the further integration of cooperative breeding and cooperation theory. Behav Proc 76:170–181

    Article  Google Scholar 

  • Brett RA (1991) The ecology of naked mole-rat colonies: burrowing, food, and limiting factors. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The biology of the naked mole-rat. Princeton University Press, Princeton, pp 137–184

    Google Scholar 

  • Carlisle TR, Zahavi A (1986) Helping at the nest, allofeeding and social status in immature Arabian babblers. Behav Ecol Sociobiol 18:339–351

    Article  Google Scholar 

  • Clarke FM, Faulkes CG (1997) Dominance and queen succession in captive colonies of the eusocial naked mole-rat, Heterocephalus glaber. Proc R Soc Lond B 264:993–1000

    CAS  Article  Google Scholar 

  • Clarke FM, Faulkes CG (2001) Intracolony aggression in the eusocial naked mole-rat, Heterocephalus glaber. Anim Behav 61:311–324

    Article  Google Scholar 

  • Clutton-Brock TH (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69–72

    CAS  Article  Google Scholar 

  • Faulkes CG, Bennett NC (2013) Plasticity and constraints on social evolution in African mole-rats: ultimate and proximate factors. Philos Trans R Soc Lond B 368:20120347

    Article  Google Scholar 

  • Jacobs DS, Jarvis JUM (1996) No evidence for the work conflict hypothesis in the eusocial naked mole-rat (Heterocephalus glaber). Behav Ecol Sociobiol 39:401–409. https://doi.org/10.1007/s002650050307

    Article  Google Scholar 

  • Jarvis JUM (1981) Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212:571–573. https://doi.org/10.1126/science.7209555

    CAS  Article  PubMed  Google Scholar 

  • Jarvis JUM, Sale JB (1971) Burrowing and burrow patterns of East African mole-rats Tachyoryctes, Heliophobius and Heterocephalus. J Zool 163:451–479. https://doi.org/10.1111/j.1469-7998.2009.00616.x

    Article  Google Scholar 

  • Koenig WD, Dickinson JL (2004) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Koenig WD, Dickinson JD (2016) Cooperative breeding in vertebrates: studies in ecology, evolution and behavior. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Kutsukake N, Inada M, Sakamoto SH, Okanoya K (2012) A distinct role of the queen in coordinated workload and soil distribution in eusocial naked mole-rats. PLoS One 7(9):e44584. https://doi.org/10.1371/journal.pone.0044584

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Lacey EA, Sherman PW (1991) Social organization of naked-mole rat colonies: evidence for the division of labor. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The biology of the naked mole-rat. Princeton University Press, Princeton, pp 275–336

    Google Scholar 

  • Lacey EA, Alexander RD, Braude SH, Sherman PW, Jarvis JUM (1991) An ethogram for the naked mole-rat: nonvocal behaviors. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The biology of the naked mole-rat. Princeton University Press, Princeton, pp 209–242

    Google Scholar 

  • Lovegrove BG (1989) The cost of burrowing by the social mole-rats (Bathyergidae) Cryptomys damarensis and Heterocephalus glaber: the role of soil moisture. Physiol Zool 62:449–469

    Article  Google Scholar 

  • Mooney SJ, Douglas NR, Holmes MM (2014) Peripheral administration of oxytocin increases social affiliation in the naked mole-rat (Heterocephalus glaber). Horm Behav 65:380–385

    CAS  Article  Google Scholar 

  • Reeve HK (1992) Queen activation of lazy workers in colonies of the eusocial naked mole-rat. Nature 358:147–149. https://doi.org/10.1038/358147a0

    CAS  Article  PubMed  Google Scholar 

  • Reeve HK, Sherman PW (1991) Intracolonial aggression and nepotism by the breeding female naked mole-rat. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The biology of the naked mole-rat. Princeton University Press, Princeton, pp 337–357

    Google Scholar 

  • Reyer H-U (1980) Flexible helper structure as an ecological adaptation in the pied kingfisher (Ceryle rudis rudis L.). Behav Ecol Sociobiol 6:219–227

    Article  Google Scholar 

  • Sherman PW, Jarvis JUM, Alexander RD (1991) The biology of the naked mole-rat. Princeton University Press, Princeton, p 344

    Google Scholar 

  • Solomon NG, French JA (1997) Cooperative breeding in mammals. Cambridge University Press, Cambridge

    Google Scholar 

  • Stacey PB, Koenig WD (1990) Cooperative breeding in birds: long-term studies of ecology and behavior. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Wright J (1997) Helping-at-the-nest in Arabian babblers: signalling social status or sensible investment in chicks? Anim Behav 54:1439–1448

    CAS  Article  Google Scholar 

  • Wright J (1999) Altruism as a signal: Zahavi’s alternative to kin selection and reciprocity. J Avian Biol 30:108–115

    Article  Google Scholar 

  • Zahavi A (1995) Altruism as a handicap: limitations of kin selection and reciprocity. J Avian Biol 26:1–3

    Article  Google Scholar 

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Acknowledgements

We thank S. Yoshida and S. Nambu for their support over the course of this study. We also thank K. Miura for providing a video clip of mole rat tail-tugging behaviour. This study was supported financially by the Japan Society for the Promotion of Science, the Special Postdoctoral Researcher program at RIKEN, the ESB Cooperation Program, SOKENDAI (the Graduate University for Advanced Studies), and Japan Science and Technology Agency, Ministry of Education, Culture, Sports, Science and Technology (MEXT; grant numbers 18870025, 2077023).

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Authors and Affiliations

  1. Department of Evolutionary Studies of Biosystems, Sokendai, The Graduate University for Advanced Studies, Hayama, Japan

    Nobuyuki Kutsukake & Shinsuke H. Sakamoto

  2. Laboratory for Biolinguistics, RIKEN Brain Science Institute, Wako, Japan

    Nobuyuki Kutsukake, Masayuki Inada & Kazuo Okanoya

  3. Department of Animal and Grassland Sciences, University of Miyazaki, Miyazaki, Japan

    Shinsuke H. Sakamoto

  4. Department of Cognitive and Behavioral Science, The University of Tokyo, Tokyo, Japan

    Kazuo Okanoya

Authors
  1. Nobuyuki Kutsukake
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  2. Masayuki Inada
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  3. Shinsuke H. Sakamoto
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  4. Kazuo Okanoya
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Corresponding author

Correspondence to Nobuyuki Kutsukake.

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Supplementary material 2 (MOV 80439 kb) ESM 2: Video of tail-tugging behaviour

Supplementary material 1 (XLSX 79 kb) ESM 1: All data

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Kutsukake, N., Inada, M., Sakamoto, S.H. et al. Behavioural interference among eusocial naked mole rats during work. J Ethol 37, 101–109 (2019). https://doi.org/10.1007/s10164-018-0581-9

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  • DOI: https://doi.org/10.1007/s10164-018-0581-9

Keywords

  • Eusociality
  • Cooperation
  • Heterocephalus glaber
  • Tail-tugging
  • Conflict