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...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2019-11-01
|
| Series: | Frontiers in Physiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fphys.2019.01426/full |
| _version_ | 1818339988399456256 |
|---|---|
| author | Marion Javal Saskia Thomas Philipp Lehmann Philipp Lehmann Madeleine G. Barton Desmond E. Conlong Desmond E. Conlong Anton Du Plessis Anton Du Plessis John S. Terblanche |
| author_facet | Marion Javal Saskia Thomas Philipp Lehmann Philipp Lehmann Madeleine G. Barton Desmond E. Conlong Desmond E. Conlong Anton Du Plessis Anton Du Plessis John S. Terblanche |
| author_sort | Marion Javal |
| collection | DOAJ |
| 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 (CTmax) 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. |
| first_indexed | 2024-12-13T15:35:45Z |
| format | Article |
| id | doaj.art-676f81c717fb4154816f648e16e8b0d8 |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-12-13T15:35:45Z |
| publishDate | 2019-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-676f81c717fb4154816f648e16e8b0d82022-12-21T23:40:02ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2019-11-011010.3389/fphys.2019.01426482274The Effect of Oxygen Limitation on a Xylophagous Insect’s Heat Tolerance Is Influenced by Life-Stage Through Variation in Aerobic Scope and Respiratory AnatomyMarion Javal0Saskia Thomas1Philipp Lehmann2Philipp Lehmann3Madeleine G. Barton4Desmond E. Conlong5Desmond E. Conlong6Anton Du Plessis7Anton Du Plessis8John S. Terblanche9Department of Conservation Ecology & Entomology, Faculty of AgriSciences, Centre for Invasion Biology, Stellenbosch University, Stellenbosch, South AfricaDepartment of Conservation Ecology & Entomology, Faculty of AgriSciences, Centre for Invasion Biology, Stellenbosch University, Stellenbosch, South AfricaDepartment of Conservation Ecology & Entomology, Faculty of AgriSciences, Centre for Invasion Biology, Stellenbosch University, Stellenbosch, South AfricaDepartment of Zoology, Stockholm University, Stockholm, SwedenDepartment of Conservation Ecology & Entomology, Faculty of AgriSciences, Centre for Invasion Biology, Stellenbosch University, Stellenbosch, South AfricaDepartment of Conservation Ecology & Entomology, Faculty of AgriSciences, Centre for Invasion Biology, Stellenbosch University, Stellenbosch, South AfricaSouth African Sugarcane Research Institute, Mount Edgecombe, South AfricaCT Scanner Facility, Central Analytical Facilities, Stellenbosch University, Stellenbosch, South AfricaPhysics Department, Stellenbosch University, Stellenbosch, South AfricaDepartment of Conservation Ecology & Entomology, Faculty of AgriSciences, Centre for Invasion Biology, Stellenbosch University, Stellenbosch, South AfricaTemperature 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 (CTmax) 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.https://www.frontiersin.org/article/10.3389/fphys.2019.01426/fullCacosceles newmanniithermolimit respirometrycritical temperaturetracheal systemhypoxia |
| spellingShingle | Marion Javal Saskia Thomas Philipp Lehmann Philipp Lehmann Madeleine G. Barton Desmond E. Conlong Desmond E. Conlong Anton Du Plessis Anton Du Plessis John S. Terblanche 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 Frontiers in Physiology Cacosceles newmannii thermolimit respirometry critical temperature tracheal system hypoxia |
| 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 | Cacosceles newmannii thermolimit respirometry critical temperature tracheal system hypoxia |
| url | https://www.frontiersin.org/article/10.3389/fphys.2019.01426/full |
| work_keys_str_mv | AT marionjaval theeffectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT saskiathomas theeffectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT philipplehmann theeffectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT philipplehmann theeffectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT madeleinegbarton theeffectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT desmondeconlong theeffectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT desmondeconlong theeffectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT antonduplessis theeffectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT antonduplessis theeffectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT johnsterblanche theeffectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT marionjaval effectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT saskiathomas effectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT philipplehmann effectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT philipplehmann effectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT madeleinegbarton effectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT desmondeconlong effectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT desmondeconlong effectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT antonduplessis effectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT antonduplessis effectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy AT johnsterblanche effectofoxygenlimitationonaxylophagousinsectsheattoleranceisinfluencedbylifestagethroughvariationinaerobicscopeandrespiratoryanatomy |