Oxygen limitation is not the cause of death during lethal heat exposure in an insect

Lehmann, Philipp; Javal, Marion; Terblanche, John S.

doi:10.1098/rsbl.2018.0701

Cited by 13 publications

(6 citation statements)

References 14 publications

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“…3D). These manipulated O 2 levels are within the P O2 range reported for the intact insect (4-10 kPa in a flight muscle of resting hawkmoth: Komai, 1998; ∼6.3±2.3 kPa in the haemolymph of a lepidopteran pupa during continuous gas exchange: P. G. D. Matthews, personal communication; see also Lehmann et al, 2019). This result could explain the previously reported high CO 2 threshold (20%) in a study which used a thoracic ganglia preparation bathed in hyperoxic saline (50% O 2 ; Bustami et al, 2002).…”

Section: Discussionsupporting

confidence: 77%

Respiratory gas levels interact to control ventilatory motor patterns in isolated locust ganglia

Talal

Ayali

Gefen

2019

Journal of Experimental Biology

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Large insects actively ventilate their tracheal system even at rest, using abdominal pumping movements, which are controlled by a central pattern generator (CPG) in the thoracic ganglia. We studied the effects of respiratory gases on the ventilatory rhythm by isolating the thoracic ganglia and perfusing its main tracheae with various respiratory gas mixtures. Fictive ventilation activity was recorded from motor nerves controlling spiracular and abdominal ventilatory muscles. Both hypoxia and hypercapnia increased the ventilation rate, with the latter being much more potent. Sub-threshold hypoxic and hypercapnic levels were still able to modulate the rhythm as a result of interactions between the effects of the two respiratory gases. Additionally, changing the oxygen levels in the bathing saline affected ventilation rate, suggesting a modulatory role for haemolymph oxygen. Central sensing of both respiratory gases as well as interactions of their effects on the motor output of the ventilatory CPG reported here indicate convergent evolution of respiratory control among terrestrial animals of distant taxa.

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Section: Discussionsupporting

confidence: 77%

Respiratory gas levels interact to control ventilatory motor patterns in isolated locust ganglia

Talal

Ayali

Gefen

2019

Journal of Experimental Biology

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“…Many aquatic species conform to one or several predictions derived from the OCLTT hypothesis (Pörtner, 2010). The results for terrestrial insects, however, remain somewhat equivocal with some species showing strong support (Woods and Hill, 2004; Boardman and Terblanche, 2015), some showing partial support (Stevens et al, 2010) and others showing little or no support (Klok et al, 2004; Lehmann et al, 2019b; reviewed in Verberk et al, 2016b). This hypothesis has proven controversial and is the focus of several recent discussions questioning, in particular, the appropriate methods for falsifying predictions thereof (Clark et al, 2013; Jutfelt et al, 2014; Pörtner, 2014) and how widespread the evidence might be supporting OCLTT across diverse taxa (Verberk et al, 2016b; Jutfelt et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2019

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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.

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“…Semsar‐Kazerouni et al., 2020; Verberk et al., 2023). The high efficiency of the tracheal system for oxygen transport has been used to explain why oxygen limitation is less evident in air breathers (Klok et al., 2004; Lehmann et al., 2019; McCue & De Los Santos, 2013; Teague et al., 2017; Verberk et al., 2016; Youngblood et al., 2019). Our study provides clear evidence that oxygen indeed affects thermal tolerance.…”

Section: Discussionmentioning

confidence: 99%

Intraspecific variation of heat tolerance in a model ectotherm: The role of oxygen, cell size and body size

Leiva,

Santos,

Rezende

et al. 2023

Functional Ecology

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Virtually all aspects of the biology of ectotherms are size‐and temperature‐dependent. Aerobic metabolism is often proposed to explain such relationships, with oxygen limitation setting limits to heat tolerance and constraining growth. However, experimental tests of the role of oxygen in heat tolerance have yielded mixed results, suggesting that oxygen limitation may be important only in certain contexts and on certain time scales but not others. Here, using thermal death time curves, which incorporate the intensity and duration of heat stress, we quantify the ability to survive heat stress in multiple inbred lines of Drosophila melanogaster, under normal and low oxygen conditions. The lines were selected to differ markedly in body size and cell size, as these traits have been hypothesised to shape thermal tolerance via their effects on oxygen supply and demand. Low oxygen condition markedly reduced survival time across inbred lines, especially when flies were exposed to prolonged, mild heat stress. Variations in heat tolerance among lines were partly related to cell size and body size differences, especially under chronic exposure to high temperatures, under hypoxia and in flies that exhibit larger cell size, supporting the idea that differences in cell size affect the oxygen supply and demand via differences in surface area to volume ratio. Because differences in heat tolerance were manifested at different timescales, our results underscore the need to close the gap between responses to acute timescales, typically employed in laboratory studies, and chronic timescales, which are ecologically more relevant. Read the free Plain Language Summary for this article on the Journal blog.

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Oxygen limitation is not the cause of death during lethal heat exposure in an insect

Cited by 13 publications

References 14 publications

Respiratory gas levels interact to control ventilatory motor patterns in isolated locust ganglia

Respiratory gas levels interact to control ventilatory motor patterns in isolated locust ganglia

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

Intraspecific variation of heat tolerance in a model ectotherm: The role of oxygen, cell size and body size

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