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Intermolt development reduces oxygen delivery capacity and jumping performance in the American locust (Schistocerca americana)

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Abstract

Among animals, insects have the highest mass-specific metabolic rates; yet, during intermolt development the tracheal respiratory system cannot meet the increased oxygen demand of older stage insects. Using locomotory performance indices, whole body respirometry, and X-ray imaging to visualize the respiratory system, we tested the hypothesis that due to the rigid exoskeleton, an increase in body mass during the intermolt period compresses the air-filled tracheal system, thereby, reducing oxygen delivery capacity in late stage insects. Specifically, we measured air sac ventilation frequency, size, and compressibility in both the abdomen and femur of early, middle, and late stage sixth instar Schistocerca americana grasshoppers. Our results show that late stage grasshoppers have a reduced air sac ventilation frequency in the femur and decreased convective capacities in the abdomen and femur. We also used X-ray images of the abdomen and femur to calculate the total proportion of tissue dedicated to respiratory structure during the intermolt period. We found that late stage grasshoppers had a lower proportion of their body dedicated to respiratory structures, especially air sacs, which convectively ventilate the tracheal system. These intermolt changes make oxygen delivery more challenging to the tissues, especially critical ones such as the jumping muscle. Indeed, late stage grasshoppers showed reduced jump frequencies compared to early stage grasshoppers, as well as decreased mass-specific CO2 emission rates at 3 kPa PO2. Our findings provide a mechanism to explain how body mass changes during the intermolt period reduce oxygen delivery capacity and alter an insect’s life history.

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Acknowledgments

Support for this project was provided by the Union College Faculty Research Fund (SDK), National Science Foundation IOS-0953297 (KJG), and National Institutes of Health 2P20RR0l5566 from the National Center for Research Resources (KJG). The contents of this study are solely the responsibility of the authors and do not necessarily reflect the views of the NIH. Use of the Advanced Photon Source at Argonne National Laboratory was supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences, under Contract DE-AC02-06CH11357. We would also like to thank Leah Pepe and Kathryn Jackson for assistance with data collection. We would like thank the three anonymous reviewers for their helpful comments in improving the manuscript.

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Authors and Affiliations

  1. Department of Biological Sciences, Union College, Schenectady, NY, 12308, USA

    Scott D. Kirkton, Lauren E. Hennessey & Bridget Duffy

  2. Department of Biological Sciences, North Dakota State University, Fargo, ND, 58108, USA

    Meghan M. Bennett & Kendra J. Greenlee

  3. X-Ray Science Division, Advanced Photon Source, Argonne National Laboratory, Argonne, IL, 60439, USA

    Wah-Keat Lee

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  1. Scott D. Kirkton
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  2. Lauren E. Hennessey
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  5. Wah-Keat Lee
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Correspondence to Scott D. Kirkton.

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Communicated by H.V. Carey.

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Kirkton, S.D., Hennessey, L.E., Duffy, B. et al. Intermolt development reduces oxygen delivery capacity and jumping performance in the American locust (Schistocerca americana). J Comp Physiol B 182, 217–230 (2012). https://doi.org/10.1007/s00360-011-0615-x

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