Isometric spiracular scaling in scarab beetles: implications for diffusive and advective oxygen transport

  1. Julian M Wagner
  2. C. Jaco Klok
  3. Meghan E Duell
  4. John J Socha
  5. Guohua Cao
  6. Hao Gong
  7. Jon Fewell Harrison  Is a corresponding author
  1. Arizona State University, United States
  2. Virginia Tech, United States
  3. ShanghaiTech University, China
  4. Mayo Clinic, United States

Abstract

The scaling of respiratory structures has been hypothesized to be a major driving factor in the evolution of many aspects of animal physiology. Here we provide the first assessment of the scaling of the spiracles in insects using ten scarab beetle species differing 180x in mass, including some of the most massive extant insect species. Using X-ray microtomography, we measured the cross-sectional area and depth of all eight spiracles, enabling the calculation of their diffusive and advective capacities. Each of these metrics scaled with geometric isometry. Because diffusive capacities scale with lower slopes than metabolic rates, the largest beetles measured require 10-fold higher PO2 gradients across the spiracles to sustain metabolism by diffusion compared to the smallest species. Large beetles can exchange sufficient oxygen for resting metabolism by diffusion across the spiracles, but not during flight. In contrast, spiracular advective capacities scale similarly or more steeply than metabolic rates, so spiracular advective capacities should match or exceed respiratory demands in the largest beetles. These data illustrate a general principle of gas exchange: scaling of respiratory transport structures with geometric isometry diminishes the potential for diffusive gas exchange but enhances advective capacities; combining such structural scaling with muscle-driven ventilation allows larger animals to achieve high metabolic rates when active.

Data availability

All data are provided in the supplementary tables.

Article and author information

Author details

  1. Julian M Wagner

    School of Life Sciences, Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. C. Jaco Klok

    School of Life Sciences, Arizona State University, Henderson, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Meghan E Duell

    School of Life Sciences, Arizona State University, Tempe, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. John J Socha

    Virginia Tech, Blacksburg, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4465-1097
  5. Guohua Cao

    School of Biomedical Engineering, ShanghaiTech University, Shanghei, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Hao Gong

    Department of Radiology, Mayo Clinic, Rochester, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Jon Fewell Harrison

    School of Life Sciences, Arizona State University, Tempe, United States
    For correspondence
    j.harrison@asu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5223-216X

Funding

NSF (IOS 1122157)

  • Jon Fewell Harrison

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. George H Perry, Pennsylvania State University, United States

Version history

  1. Preprint posted: April 8, 2022 (view preprint)
  2. Received: July 24, 2022
  3. Accepted: August 16, 2022
  4. Accepted Manuscript published: September 13, 2022 (version 1)
  5. Version of Record published: September 29, 2022 (version 2)
  6. Version of Record updated: September 30, 2022 (version 3)

Copyright

© 2022, Wagner et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Julian M Wagner
  2. C. Jaco Klok
  3. Meghan E Duell
  4. John J Socha
  5. Guohua Cao
  6. Hao Gong
  7. Jon Fewell Harrison
(2022)
Isometric spiracular scaling in scarab beetles: implications for diffusive and advective oxygen transport
eLife 11:e82129.
https://doi.org/10.7554/eLife.82129

Share this article

https://doi.org/10.7554/eLife.82129

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