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      Revealing the respiratory system of the coffee berry borer ( Hypothenemus hampei; Coleoptera: Curculionidae: Scolytinae) using micro-computed tomography

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          Abstract

          The coffee berry borer ( Hypothenemus hampei) is the most economically important insect pest of coffee globally. Micro-computed tomography (micro-CT) was used to reconstruct the respiratory system of this species for the first time; this is the smallest insect (ca. 2 mm long) for which this has been done to date. Anatomical details of the spiracles and tracheal tubes are described, images presented, and new terms introduced. The total volume and the relationship between tracheal lumen diameter, length and volume are also presented. The total length of the tracheal tubes are seventy times the length of the entire animal. Videos and a 3D model for use with mobile devices are included as supplementary information; these could be useful for future research and for teaching insect anatomy to students and the public in general.

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          Tracheal respiration in insects visualized with synchrotron x-ray imaging.

          Richard Blob, Kamel Fezzaa, Keat Lee … (2003)
          Insects are known to exchange respiratory gases in their system of tracheal tubes by using either diffusion or changes in internal pressure that are produced through body motion or hemolymph circulation. However, the inability to see inside living insects has limited our understanding of their respiration mechanisms. We used a synchrotron beam to obtain x-ray videos of living, breathing insects. Beetles, crickets, and ants exhibited rapid cycles of tracheal compression and expansion in the head and thorax. Body movements and hemolymph circulation cannot account for these cycles; therefore, our observations demonstrate a previously unknown mechanism of respiration in insects analogous to the inflation and deflation of vertebrate lungs.
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            Increase in tracheal investment with beetle size supports hypothesis of oxygen limitation on insect gigantism.

            C Jaco Klok, Alexander Kaiser, P. Harrison … (2007)
            Recent studies have suggested that Paleozoic hyperoxia enabled animal gigantism, and the subsequent hypoxia drove a reduction in animal size. This evolutionary hypothesis depends on the argument that gas exchange in many invertebrates and skin-breathing vertebrates becomes compromised at large sizes because of distance effects on diffusion. In contrast to vertebrates, which use respiratory and circulatory systems in series, gas exchange in insects is almost exclusively determined by the tracheal system, providing a particularly suitable model to investigate possible limitations of oxygen delivery on size. In this study, we used synchrotron x-ray phase-contrast imaging to visualize the tracheal system and quantify its dimensions in four species of darkling beetles varying in mass by 3 orders of magnitude. We document that, in striking contrast to the pattern observed in vertebrates, larger insects devote a greater fraction of their body to the respiratory system, as tracheal volume scaled with mass1.29. The trend is greatest in the legs; the cross-sectional area of the trachea penetrating the leg orifice scaled with mass1.02, whereas the cross-sectional area of the leg orifice scaled with mass0.77. These trends suggest the space available for tracheae within the leg may ultimately limit the maximum size of extant beetles. Because the size of the tracheal system can be reduced when oxygen supply is increased, hyperoxia, as occurred during late Carboniferous and early Permian, may have facilitated the evolution of giant insects by allowing limbs to reach larger sizes before the tracheal system became limited by spatial constraints.
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              Episodes in insect evolution.

              Steven Reppert, Robert Dudley, John VandenBrooks … (2009)
              This article derives from a society-wide symposium organized by Timothy Bradley and Adriana Briscoe and presented at the 2009 annual meeting of the Society for Integrative and Comparative Biology in Boston, Massachusetts. David Grimaldi provided the opening presentation in which he outlined the major evolutionary events in the formation and subsequent diversification of the insect clade. This presentation was followed by speakers who detailed the evolutionary history of specific physiological and/or behavioral traits that have caused insects to be both ecologically successful and fascinating as subjects for biological study. These include a review of the evolutionary history of the insects, the origins of flight, osmoregulation, the evolution of tracheal systems, the evolution of color vision, circadian clocks, and the evolution of eusociality. These topics, as covered by the speakers, provide an overview of the pattern and timing of evolutionary diversification and specialization in the group of animals we know as insects.
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                Author and article information

                Contributors
                Javier Alba-Tercedor: jalba@ugr.es
                Fernando E. Vega: Fernando.Vega@usda.gov
                Journal
                Journal ID (nlm-ta): Sci Rep
                Journal ID (iso-abbrev): Sci Rep
                Title: Scientific Reports
                Publisher: Nature Publishing Group UK (London )
                ISSN (Electronic): 2045-2322
                Publication date (Electronic): 28 November 2019
                Publication date PMC-release: 28 November 2019
                Publication date Collection: 2019
                Volume: 9
                Electronic Location Identifier: 17753
                Affiliations
                [1 ]ISNI 0000000121678994, GRID grid.4489.1, Department of Zoology, Faculty of Sciences, , University of Granada, Campus de Fuentenueva, ; 18071 Granada, Spain
                [2 ]ISNI 0000 0004 0404 0958, GRID grid.463419.d, Sustainable Perennial Crops Laboratory, United States Department of Agriculture, , Agricultural Research Service, ; Beltsville, MD 20705 USA
                Article
                Publisher ID: 54157
                DOI: 10.1038/s41598-019-54157-3
                PMC ID: 6882887
                PubMed ID: 31780747
                SO-VID: f7a711ce-898a-4afb-ab26-ab5f7451bd96
                Copyright statement: © The Author(s) 2019
                License:

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                Date received : 8 August 2019
                Date accepted : 30 October 2019
                Funding
                Funded by: Sub-award agreement S15192.01 between Kansas State University (KSU) and the University of Granada, as part of a USDA-NIFA Award 2014-70016-23028 to S. J. Brown (KSU)
                Categories
                Subject: Article
                Custom metadata
                issue-copyright-statement © The Author(s) 2019

                ScienceOpen disciplines: Uncategorized
                Keywords: biological techniques,zoology
                Data availability:
                ScienceOpen disciplines: Uncategorized
                Keywords: biological techniques, zoology

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