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The Effect of Oxygen Limitation on a Xylophagous Insect’s Heat Tolerance Is Influenced by Life-Stage Through Variation in Aerobic Scope and Respiratory Anatomy

Temperature has a profound impact on insect fitness and performance via metabolic, enzymatic or chemical reaction rate effects. However, oxygen availability can interact with these thermal responses in complex and often poorly understood ways, especially in hypoxia-adapted species. Here we test the...

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Autores principales: Javal, Marion, Thomas, Saskia, Lehmann, Philipp, Barton, Madeleine G., Conlong, Desmond E., Du Plessis, Anton, Terblanche, John S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6879455/
https://www.ncbi.nlm.nih.gov/pubmed/31824337
http://dx.doi.org/10.3389/fphys.2019.01426
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author Javal, Marion
Thomas, Saskia
Lehmann, Philipp
Barton, Madeleine G.
Conlong, Desmond E.
Du Plessis, Anton
Terblanche, John S.
author_facet Javal, Marion
Thomas, Saskia
Lehmann, Philipp
Barton, Madeleine G.
Conlong, Desmond E.
Du Plessis, Anton
Terblanche, John S.
author_sort Javal, Marion
collection PubMed
description Temperature has a profound impact on insect fitness and performance via metabolic, enzymatic or chemical reaction rate effects. However, oxygen availability can interact with these thermal responses in complex and often poorly understood ways, especially in hypoxia-adapted species. Here we test the hypothesis that thermal limits are reduced under low oxygen availability – such as might happen when key life-stages reside within plants – but also extend this test to attempt to explain that the magnitude of the effect of hypoxia depends on variation in key respiration-related parameters such as aerobic scope and respiratory morphology. Using two life-stages of a xylophagous cerambycid beetle, Cacosceles (Zelogenes) newmannii we assessed oxygen-limitation effects on metabolic performance and thermal limits. We complement these physiological assessments with high-resolution 3D (micro-computed tomography scan) morphometry in both life-stages. Results showed that although larvae and adults have similar critical thermal maxima (CT(max)) under normoxia, hypoxia reduces metabolic rate in adults to a greater extent than it does in larvae, thus reducing aerobic scope in the former far more markedly. In separate experiments, we also show that adults defend a tracheal oxygen (critical) setpoint more consistently than do larvae, indicated by switching between discontinuous gas exchange cycles (DGC) and continuous respiratory patterns under experimentally manipulated oxygen levels. These effects can be explained by the fact that the volume of respiratory anatomy is positively correlated with body mass in adults but is apparently size-invariant in larvae. Thus, the two life-stages of C. newmannii display key differences in respiratory structure and function that can explain the magnitude of the effect of hypoxia on upper thermal limits.
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spelling pubmed-68794552019-12-10 The Effect of Oxygen Limitation on a Xylophagous Insect’s Heat Tolerance Is Influenced by Life-Stage Through Variation in Aerobic Scope and Respiratory Anatomy Javal, Marion Thomas, Saskia Lehmann, Philipp Barton, Madeleine G. Conlong, Desmond E. Du Plessis, Anton Terblanche, John S. Front Physiol Physiology Temperature has a profound impact on insect fitness and performance via metabolic, enzymatic or chemical reaction rate effects. However, oxygen availability can interact with these thermal responses in complex and often poorly understood ways, especially in hypoxia-adapted species. Here we test the hypothesis that thermal limits are reduced under low oxygen availability – such as might happen when key life-stages reside within plants – but also extend this test to attempt to explain that the magnitude of the effect of hypoxia depends on variation in key respiration-related parameters such as aerobic scope and respiratory morphology. Using two life-stages of a xylophagous cerambycid beetle, Cacosceles (Zelogenes) newmannii we assessed oxygen-limitation effects on metabolic performance and thermal limits. We complement these physiological assessments with high-resolution 3D (micro-computed tomography scan) morphometry in both life-stages. Results showed that although larvae and adults have similar critical thermal maxima (CT(max)) under normoxia, hypoxia reduces metabolic rate in adults to a greater extent than it does in larvae, thus reducing aerobic scope in the former far more markedly. In separate experiments, we also show that adults defend a tracheal oxygen (critical) setpoint more consistently than do larvae, indicated by switching between discontinuous gas exchange cycles (DGC) and continuous respiratory patterns under experimentally manipulated oxygen levels. These effects can be explained by the fact that the volume of respiratory anatomy is positively correlated with body mass in adults but is apparently size-invariant in larvae. Thus, the two life-stages of C. newmannii display key differences in respiratory structure and function that can explain the magnitude of the effect of hypoxia on upper thermal limits. Frontiers Media S.A. 2019-11-20 /pmc/articles/PMC6879455/ /pubmed/31824337 http://dx.doi.org/10.3389/fphys.2019.01426 Text en Copyright © 2019 Javal, Thomas, Lehmann, Barton, Conlong, Du Plessis and Terblanche. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Javal, Marion
Thomas, Saskia
Lehmann, Philipp
Barton, Madeleine G.
Conlong, Desmond E.
Du Plessis, Anton
Terblanche, John S.
The Effect of Oxygen Limitation on a Xylophagous Insect’s Heat Tolerance Is Influenced by Life-Stage Through Variation in Aerobic Scope and Respiratory Anatomy
title The Effect of Oxygen Limitation on a Xylophagous Insect’s Heat Tolerance Is Influenced by Life-Stage Through Variation in Aerobic Scope and Respiratory Anatomy
title_full The Effect of Oxygen Limitation on a Xylophagous Insect’s Heat Tolerance Is Influenced by Life-Stage Through Variation in Aerobic Scope and Respiratory Anatomy
title_fullStr The Effect of Oxygen Limitation on a Xylophagous Insect’s Heat Tolerance Is Influenced by Life-Stage Through Variation in Aerobic Scope and Respiratory Anatomy
title_full_unstemmed The Effect of Oxygen Limitation on a Xylophagous Insect’s Heat Tolerance Is Influenced by Life-Stage Through Variation in Aerobic Scope and Respiratory Anatomy
title_short The Effect of Oxygen Limitation on a Xylophagous Insect’s Heat Tolerance Is Influenced by Life-Stage Through Variation in Aerobic Scope and Respiratory Anatomy
title_sort effect of oxygen limitation on a xylophagous insect’s heat tolerance is influenced by life-stage through variation in aerobic scope and respiratory anatomy
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6879455/
https://www.ncbi.nlm.nih.gov/pubmed/31824337
http://dx.doi.org/10.3389/fphys.2019.01426
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