Abstract

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.

Highlights

  • Temperature is a key environmental driver of insect population dynamics since it directly affects life-history traits (Angilletta, 2009)

  • We investigated whether oxygen availability influenced upper critical (=lethal) temperature through thermolimit respirometry (TLR; Lighton and Turner, 2004) in larvae and adults under normoxia and hypoxia

  • Assuming that discontinuous gas exchange cycles (DGC, i.e., showing a clear prolonged spiracle-closed phase) are undertaken to defend a particular tracheal respiratory pO2 setpoint of 4– 5 kPa, we investigated whether respiration patterns were affected by variation in ambient oxygen availability

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Summary

INTRODUCTION

Temperature is a key environmental driver of insect population dynamics since it directly affects life-history traits (Angilletta, 2009). Larvae on the other hand are expected to be more hypoxia-tolerant due to their saproxylic or wood-boring nature but to perhaps have limited aerobic scope since their activities do not imply large energy expenditure at this stage (e.g., they lack flight ability) Overall, these differences are expected to be associated with structural differences in the tracheal system (i.e., respiratory anatomy): in conditions of constant energy demand, adults would have a more developed tracheal system (estimated as e.g., total air volume) relative to their body size compared to larvae, indicative of greater potential upper capacity for oxygen flux (supply). Using a combination of experimental respirometry and 3D-imaging of respiratory anatomy, we investigate functional hypoxia and temperature tolerance in a member of a previously unexamined group of terrestrial arthropods

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