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Research Article

Self-organized biotectonics of termite nests

View ORCID ProfileAlexander Heyde, View ORCID ProfileLijie Guo, View ORCID ProfileChristian Jost, View ORCID ProfileGuy Theraulaz, and View ORCID ProfileL. Mahadevan
PNAS February 2, 2021 118 (5) e2006985118; https://doi.org/10.1073/pnas.2006985118
Alexander Heyde
aDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138;
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Lijie Guo
bCentre de Recherches sur la Cognition Animale, Centre de Biologie Intégrative, Université de Toulouse, CNRS, Université de Toulouse–Paul Sabatier, 31062 Toulouse France;
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Christian Jost
bCentre de Recherches sur la Cognition Animale, Centre de Biologie Intégrative, Université de Toulouse, CNRS, Université de Toulouse–Paul Sabatier, 31062 Toulouse France;
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Guy Theraulaz
bCentre de Recherches sur la Cognition Animale, Centre de Biologie Intégrative, Université de Toulouse, CNRS, Université de Toulouse–Paul Sabatier, 31062 Toulouse France;
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L. Mahadevan
aDepartment of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138;
cSchool of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138;
dDepartment of Physics, Harvard University, Cambridge, MA 02138
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  • For correspondence: lmahadev@g.harvard.edu
  1. Edited by Simon A. Levin, Princeton University, Princeton, NJ, and approved November 16, 2020 (received for review April 16, 2020)

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Significance

Termite nests are a remarkable example of functional self-organization that show how structure and function emerge on multiple length and time scales in ecophysiology. To understand the process by which this arises, we document the labyrinthine architecture within the subterranean nests of the African termite Apicotermes lamani and develop a simple mathematical model that relies on the physical and biological interactions between termites, pheromones, and mud in the nest. Our model explains the formation of parallel floors connected by linear and helical ramps, consistent with observations of real nests. In describing this multiagent system, we elucidate principles of physical and behavioral coupling with relevance to swarm intelligence and architectural design.

Abstract

The termite nest is one of the architectural wonders of the living world, built by the collective action of workers in a colony. Each nest has several characteristic structural motifs that allow for efficient ventilation, cooling, and traversal. We use tomography to quantify the nest architecture of the African termite Apicotermes lamani, consisting of regularly spaced floors connected by scattered linear and helicoidal ramps. To understand how these elaborate structures are built and arranged, we formulate a minimal model for the spatiotemporal evolution of three hydrodynamic fields—mud, termites, and pheromones—linking environmental physics to collective building behavior using simple local rules based on experimental observations. We find that floors and ramps emerge as solutions of the governing equations, with statistics consistent with observations of A. lamani nests. Our study demonstrates how a local self-reinforcing biotectonic scheme is capable of generating an architecture that is simultaneously adaptable and functional, and likely to be relevant for a range of other animal-built structures.

  • collective animal behavior
  • termite nests
  • stigmergy
  • ecophysiology
  • morphogenesis

Footnotes

  • ↵1To whom correspondence may be addressed. Email: lmahadev{at}g.harvard.edu.
  • Author contributions: A.H., G.T., and L.M. designed research; A.H. and L.M. performed research; A.H., L.G., C.J., G.T., and L.M. contributed new reagents/analytic tools; A.H., L.G., C.J., and L.M. analyzed data; and A.H., G.T., and L.M. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2006985118/-/DCSupplemental.

Data Availability.

The HTML three-dimensional images and Datasets S1 and S2 have been deposited in Harvard Dataverse (https://doi.org/10.7910/DVN/Z1GWTI) (32).

Published under the PNAS license.

View Full Text

References

  1. ↵
    1. M. Hansell
    , Animal Architecture (Oxford University Press, 2005).
  2. ↵
    1. A. Perna,
    2. G. Theraulaz
    , When social behavior is molded in clay: On growth and form of social insect nests. J. Exp. Biol. 220, 83–91 (2017).
    OpenUrlAbstract/FREE Full Text
  3. ↵
    1. C. C. Lee,
    2. K. B. Neoh,
    3. C. Y. Lee
    , Caste composition and mound size of the subterranean termite macrotermes gilvus (isoptera: Termitidae: Macrotermitinae). Ann. Entomol. Soc. Am. 105, 427–433 (2012).
    OpenUrlCrossRef
  4. ↵
    1. J. S. Turner
    , On the mound of macrotermes michaelseni as an organ of respiratory gas exchange. Physiol. Biochem. Zool. 74, 798–822 (2001).
    OpenUrlCrossRefPubMed
  5. ↵
    1. H. King,
    2. S. A. Ocko,
    3. L. Mahadevan
    , Termite mounds harness diurnal temperature oscillations for ventilation. Proc. Natl. Acad. Sci. U.S.A. 112, 11589–11593 (2015).
    OpenUrlAbstract/FREE Full Text
  6. ↵
    1. et al.
    , Solar-powered ventilation of African termite mounds. J. Exp. Biol. 22, 3260–3269 (2017).
    OpenUrl
  7. ↵
    1. S Camazine et al.
    , Self-Organization in Biological Systems (Princeton University Press, 2003), vol. 7.
  8. ↵
    1. D. J. T. Sumpter
    , Collective Animal Behavior (Princeton University Press, 2010).
  9. ↵
    1. C. Anderson,
    2. D. W. McShea
    , Intermediate-level parts in insect societies: Adaptive structures that ants build away from the nest. Insectes Soc. 48, 291–301 (2001).
    OpenUrlCrossRef
  10. ↵
    1. T. J. Czaczkes,
    2. C. Grüter,
    3. F. L. W. Ratnieks
    , Trail pheromones: An integrative view of their role in social insect colony organization. Annu. Rev. Entomol. 60, 581–599 (2015).
    OpenUrlCrossRefPubMed
  11. ↵
    1. E. Bonabeau,
    2. G. Theraulaz,
    3. J. L. Deneubourg,
    4. S. Aron,
    5. S. Camazine
    . Self-organization in social insects. Trends Ecol. Evol. 12, 188–193 (1997).
    OpenUrlCrossRefPubMed
  12. ↵
    1. J. Desneux,
    2. A. E. Emerson
    , Les Constructions Hypogées des Apicotermes Termites de l’Afrique Tropicale (Musée Royale du Congo Belge, 1952), vol. 17.
  13. ↵
    1. R. S. Schmidt
    , Functions of apicotermes nests. Insectes Soc. 7, 357–368 (1960).
    OpenUrl
  14. ↵
    1. J. Korb,
    2. K. E. Linsenmair
    , The architecture of termite mounds: A result of a trade-off between thermoregulation and gas exchange?. Behav. Ecol. 10, 312–316 (1999).
    OpenUrlCrossRef
  15. ↵
    1. K. Singh et al.
    , The architectural design of smart ventilation and drainage systems in termite nests. Sci. Adv. 5, eaat8520 (2019).
    OpenUrlFREE Full Text
  16. ↵
    1. G. Theraulaz,
    2. E. Bonabeau
    , A brief history of stigmergy. Artif. Life 5, 97–116 (1999).
    OpenUrlCrossRefPubMed
  17. ↵
    1. P. P. Grassé
    , La reconstruction du nid et les coordinations interindividuelles chezbellicositermes natalensis et cubitermes sp. la théorie de la stigmergie: Essai d’interprétation du comportement des termites constructeurs. Insectes Soc. 6, 41–80 (1959).
    OpenUrlCrossRef
  18. ↵
    1. S. A. Ocko,
    2. A. Heyde,
    3. L. Mahadevan
    , Morphogenesis of termite mounds. Proc. Natl. Acad. Sci. U.S.A. 116, 3379–3384 (2019).
    OpenUrlAbstract/FREE Full Text
  19. ↵
    1. A. Khuong et al.
    , Stigmergic construction and topochemical information shape ant nest architecture. Proc. Natl. Acad. Sci. U.S.A. 113, 1303–1308 (2016).
    OpenUrlAbstract/FREE Full Text
  20. ↵
    1. O. H. Bruinsma
    . “An analysis of building behavior of the termite macrotermes subhyalinus (Rambur),” PhD thesis Landbouwhogeschool Wageningen, Wageningen, The Netherlands, (1979).
  21. ↵
    1. M. A. Biot
    , General theory of three-dimensional consolidation. J. Appl. Phys. 12, 155–164 (1941).
    OpenUrlCrossRef
  22. ↵
    1. A. Stevens
    , The derivation of chemotaxis equations as limit dynamics of moderately interacting stochastic many-particle systems. SIAM J. Appl. Math. 61, 183–212 (2000).
    OpenUrl
  23. ↵
    1. P. Amorim
    , Modeling ant foraging: A chemotaxis approach with pheromones and trail formation. J. Theor. Biol. 385, 160–173 (2015).
    OpenUrl
  24. ↵
    1. R. S. Schmidt
    , Apticotermes nests. Am. Zoologist 4, 221–225 (1964).
    OpenUrlCrossRef
  25. ↵
    1. D. Fouquet,
    2. A. M. Costa-Leonardo,
    3. R. Fournier,
    4. S. Blanco,
    5. C. Jost
    , Coordination of construction behavior in the termite Procornitermes araujoi: Structure is a stronger stimulus than volatile marking. Insectes Soc. 61, 253–264 (2014).
    OpenUrlCrossRef
  26. ↵
    1. J. P. Hirth,
    2. J. Lothe,
    3. T. Mura
    , Theory of Dislocations (Cambridge University Press, 1983).
  27. ↵
    1. A. Perna et al.
    , Topological efficiency in three-dimensional gallery networks of termite nests. Physica A 387, 6235–6244 (2008).
    OpenUrlCrossRef
  28. ↵
    1. M. D. Cox,
    2. G. B. Blanchard
    , Gaseous templates in ant nests. J. Theor. Biol. 204, 223–238 (2000).
    OpenUrlCrossRefPubMed
  29. ↵
    1. I. Wallis,
    2. L. Bilan,
    3. M. Smith,
    4. A. S. Kazi
    1. J. S. Turner,
    2. R. C. Soar
    , “Beyond biomimicry: What termites can tell us about realizing the living building” in Industrialised, Integrated, Intelligent sustainable Construction: I3CON Handbook 2, I. Wallis, L. Bilan, M. Smith, A. S. Kazi, Eds. (I3CON & BSRIA Limited, Bracknell, UK, 2010), pp. 234–248.
  30. ↵
    1. P. Villa
    , Terra Amata and the Middle Pleistocene Archeological Record of Southern France (University of California Publications in Anthropology, Berkeley, CA, 1983), vol. 13.
  31. ↵
    1. D. A. Arab et al.
    , Parallel evolution of mound-building and grass-feeding in Australian nasute termites. Biol. Lett. 13, 20160665 (2017).
    OpenUrlCrossRefPubMed
  32. ↵
    1. A. Heyde,
    2. L. Guo,
    3. C. Jost,
    4. G. Theraulaz,
    5. L. Mahadevan
    , Termite biotectonics data. Harvard Dataverse. https://doi.org/10.7910/DVN/Z1GWTI. Deposited 12 November 2020.

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Self-organized biotectonics of termite nests
Alexander Heyde, Lijie Guo, Christian Jost, Guy Theraulaz, L. Mahadevan
Proceedings of the National Academy of Sciences Feb 2021, 118 (5) e2006985118; DOI: 10.1073/pnas.2006985118

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Self-organized biotectonics of termite nests
Alexander Heyde, Lijie Guo, Christian Jost, Guy Theraulaz, L. Mahadevan
Proceedings of the National Academy of Sciences Feb 2021, 118 (5) e2006985118; DOI: 10.1073/pnas.2006985118
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  • Physical Sciences
  • Biophysics and Computational Biology
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  • Article
    • Abstract
    • Digitization and Structure of Apicotermes Nests
    • A Minimal Model of Biotectonics
    • Natural Patterns in Simulated Nests
    • Emergent Biotectonics from Physics and Behavior
    • Materials and Methods
    • Data Availability.
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