Skip to main content

Allometric scaling law and ergodicity breaking in the vascular system

Abstract

Allometry or the quantitative study of the relationship of body size to living organism physiology is an important area of biophysical scaling research. The West-Brown-Enquist (WBE) model of fractal branching in a vascular network explains the empirical allometric Kleiber law (the ¾ scaling exponent for metabolic rates as a function of animal’s mass). The WBE model raises a number of new questions, such as how to account for capillary phenomena more accurately and what are more realistic dependencies for blood flow velocity on the size of a capillary. We suggest a generalized formulation of the branching model and investigate the ergodicity in the fractal vascular system. In general, the fluid flow in such a system is not ergodic, and ergodicity breaking is attributed to the fractal structure of the network. Consequently, the fractal branching may be viewed as a source of ergodicity breaking in biophysical systems, in addition to such mechanisms as aging and macromolecular crowding. Accounting for non-ergodicity is important for a wide range of biomedical applications where long observations of time series are impractical. The relevance to microfluidics applications is also discussed.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Arnold V (1978) Mathematical methods of classical mechanics. Springer, New York

    Book  Google Scholar 

  • Arnold V, Avez A (1968) Ergodic problems of classical mechanics. Benjamin, New York

    MATH  Google Scholar 

  • Banavar JR, Moses ME, Brown JH, Damuth J, Rinaldo A, Sibly RM, Maritan A (2010) A general basis for quarter-power scaling in animals. Proc Nat Acad Sci 107(36):15816–15820

    Article  Google Scholar 

  • Bejan A (2004) The constructal law of organization in nature: tree-shaped flows and body size. J Exp Biol 208:1677–1686

    Article  Google Scholar 

  • Bejan A (2012) Why the bigger live longer and travel farther: animals, vehicles, rivers and the winds. Sci Rep 2:594

    Article  Google Scholar 

  • Birkhoff G (1931) Proof of the ergodic theorem. Proc Natl Acad Sci 17:656–660

    Article  Google Scholar 

  • Bormashenko E, Voronel A (2018) Spatial scales of living cells and their energetic and informational capacity. Eur Biophys J 47(5):515–521

    Article  Google Scholar 

  • Brown JH, West GB, Enquist BJ (2005) Yes, West, Brown and Enquist’s model of allometric scaling is both mathematically correct and biologically relevant. Funct Ecol 19(4):735–738

    Article  Google Scholar 

  • De Lellis C, Székelyhidi L (2019) On turbulence and geometry: from Nash to Onsager. Not Am Math Soc 05:677–685

    MathSciNet  MATH  Google Scholar 

  • Eloy C (2011) Leonardo’s Rule, self-similarity, and wind-Induced stresses in trees. Phys Rev Lett 107:258101

    Article  Google Scholar 

  • Etienne RS, Apol ME, Olff HA (2006) Demystifying the West, Brown & Enquist model of the allometry of metabolism. Funct Ecol 20(2):394–399

    Article  Google Scholar 

  • Fabry B, Maksym GN, Butler JP, Glogauer M, Navajas D, Taback NA, Millet EJ, Fredberg JJ (2003) Time scale and other invariants of integrative mechanical behavior in living cells. Phys Rev E 68:041914

    Article  Google Scholar 

  • Fedorets AA, Bormashenko E, Dombrovsky LA, Nosonovsky M (2019a) Droplet clusters: nature-inspired biological reactors and aerosols Phil. Trans R Soc A 377(2150):20190121

    Google Scholar 

  • Fedorets AA, Aktaev NE, Gabyshev DN, Bormashenko E, Dombrovsky LA, Nosonovsky M (2019b) Oscillatory motion of a droplet cluster. J Phys Chem C 123(38):23572–23576

    Article  Google Scholar 

  • Földes-Papp Z, Baumann G (2011) Fluorescence molecule counting for single-molecule studies in crowded environment of living cells without and with broken ergodicity. Curr Pharm Biotechnol 12(5):824–833. https://doi.org/10.2174/138920111795470949

    Article  Google Scholar 

  • Guzman-Sepulveda J, Argueta-Morales R, DeCampli WM, Dogariu A (2017) Real-time intraoperative monitoring of blood coagulability via coherence-gated light scattering. Nat Biomed Eng 1:0028. https://doi.org/10.1038/s41551-017-0028

    Article  Google Scholar 

  • Hasan A, Paul A, Vrana NE, Zhao X, Memic A, Hwang YS, Dokmeci MR, Khademhosseini A (2014) Microfluidic techniques for development of 3D vascularized tissue. Biomaterials 35:7308–7325

    Article  Google Scholar 

  • Hofling F, Franosch T (2013) Anomalous transport in the crowded world of biological cells. Rep Prog Phys 76:046602. https://doi.org/10.1088/0034-4885/76/4/046602

    Article  MathSciNet  Google Scholar 

  • Hrnčíř E, Rosina J (1997) Surface tension of blood. Physiol Res 46(4):319–321

    Google Scholar 

  • Kadanoff LP (2009) More is the same; phase transitions and mean field theories. J Stat Phys 137:777–797

    Article  MathSciNet  Google Scholar 

  • Kleiber M (1932) Body size and metabolism. Hilgardia 6(11):315–351

    Article  Google Scholar 

  • Kleiber M (1947) Body size and metabolic rate. Physiol Rev 27(4):511–541

    Article  Google Scholar 

  • Kozlowski J, Konarzewski M (2004) Is West, Brown and Enquist’s model of allometric scaling mathematically correct and biologically relevant? Funct Ecol 18(2):283–289

    Article  Google Scholar 

  • Krishnan A, Wilson A, Sturgeon J, Siedleckia CA, Vogler EA (2005) Liquid–vapor interfacial tension of blood plasma, serum and purified protein constituents thereof. Biomaterials 26(17):3445–3453

    Article  Google Scholar 

  • Kulkarni AM, Dixit NM, Zukoski CF (2003) Ergodic and non-ergodic phase transitions in globular protein suspensions. Faraday Discuss 123:37–50

    Article  Google Scholar 

  • Lim MX, Souslov A, Vitelli V, Jaeger HM (2019) Cluster formation by acoustic forces and active fluctuations in levitated granular matter. Nat Phys 15:460–464

    Article  Google Scholar 

  • Maani N, Rayz VL, Nosonovsky M (2015) Biomimetic approaches for green tribology: from the lotus effect to blood flow control. Surf Topogr Metrol Prop 3:034001

    Article  Google Scholar 

  • Magdziarz M, Zorawik T (2019) Lamperti transformation - cure for ergodicity breaking. Commun Nonlinear Sci Numer Simulat 71:202–211

    Article  MathSciNet  Google Scholar 

  • Manzo C, Torreno-Pina JA, Massignan P, Lapeyre GJ, Lewenstein M, Garcia Parajo MF (2015) Weak ergodicity breaking of receptor motion in living cells stemming from random diffusivity. Phys Rev X 5:011021

    Google Scholar 

  • Marieb EN, Hoehn K (2013) The cardiovascular system: blood vessels, 9th edn. Human anatomy & physiology. Pearson Education, London, p 712

    Google Scholar 

  • Nosonovsky M, Rohatgi PK (2012) Biomimetics in materials science: self-healing, self-lubricating, and self-cleaning materials. Springer, New York

    Book  Google Scholar 

  • Nosonovsky M, Roy P (2020) Scaling in colloidal and biological networks. Entropy 22(6):622

    Article  Google Scholar 

  • Ramachandran R, Maani N, Rayz VL, Nosonovsky M (2016) Vibrations and spatial patterns in biomimetic surfaces: using the shark-skin effect to control blood clotting. Phil Trans R Soc A 374:20160133

    Article  Google Scholar 

  • Rypina II, Scott SE, Pratt LJ, Brown MG (2011) Investigating the connection between complexity of isolated trajectories and Lagrangian coherent structures. Nonlinear Process Geophys 18:977–987

    Article  Google Scholar 

  • Savage VM, Gillooly JF, Woodruff WH, West GB, Allen AP, Enquist BJ, Brown JH (2004) The predominance of quarter-power scaling in biology. Funct Ecol 18(2):257–282

    Article  Google Scholar 

  • Savage VM, Deeds EJ, Fontana W (2008) Sizing up allometric scaling theory. PLoS Comput Biol 4(9):e1000171. https://doi.org/10.1371/journal.pcbi.1000171

    Article  MathSciNet  Google Scholar 

  • Scott SE, Redd TC, Kuznetsov L, Mezić I, Jones CKRT (2009) Capturing deviation from ergodicity at different scales. Physica D 238(16):1668–1679

    Article  MathSciNet  Google Scholar 

  • Shnirelman A (2000) Weak solutions with decreasing energy of incompressible Euler equations. Comm Math Phys 210:541–603

    Article  MathSciNet  Google Scholar 

  • Thurston GB (1976) Viscosity and viscoelasticity of blood in small diameter tubes. Microvasc Res 11:133–146

    Article  Google Scholar 

  • West GB, Brown JH, Enquist BJ (1997) A general model for the origin of allometric scaling laws in biology. Science 276(5309):122–126

    Article  Google Scholar 

  • Wolfram S (2020) Geometric Series. http://mathworld.wolfram.com/GeometricSeries.html. Accessed 20 May 2019

Download references

Acknowledgement

Partially supported by the Russian Science Foundation (project 19-19-00076). The authors would like to thank Prof. Roshan D’Souza for the CFD software used in this study and anonymous reviewers for the discussion which improved this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael Nosonovsky.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nosonovsky, M., Roy, P. Allometric scaling law and ergodicity breaking in the vascular system. Microfluid Nanofluid 24, 53 (2020). https://doi.org/10.1007/s10404-020-02359-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10404-020-02359-x

Keywords

  • Allometry
  • Ergodicity
  • Fractal branching
  • Capillaries
  • Cardiovascular system
  • Microfluidics