Oxygen safety margins set thermal limits in an insect model system

Abstract

A mismatch between oxygen availability and metabolic demand may constrain thermal tolerance. While considerable support for this idea has been found in marine organisms, results from insects are equivocal and raise the possibility that mode of gas exchange, oxygen safety margins and the physico-chemical properties of the gas medium influence heat tolerance estimates. Here, we examined critical thermal maximum (CT max ) and aerobic scope under altered oxygen supply and in two life stages that varied in metabolic demand in Bombyx mori (Lepidoptera: Bombycidae). We also systematically examined the influence of changes in gas properties on CT max . Larvae have a lower oxygen safety margin (higher critical oxygen partial pressure at which metabolism is suppressed relative to metabolic demand) and significantly higher CT max under normoxia than pupae (53°C vs 50°C). Larvae, but not pupae, were oxygen limited with hypoxia (2.5 kPa) decreasing CT max significantly from 53 to 51°C. Humidifying hypoxic air relieved the oxygen limitation effect on CT max in larvae, whereas variation in other gas properties did not affect CT max . Our data suggest that oxygen safety margins set thermal limits in air-breathing invertebrates and the magnitude of this effect potentially reconciles differences in oxygen limitation effects on thermal tolerance found among diverse taxa to date.

Thermal limits in native and alien freshwater peracarid Crustacea: The role of habitat use and oxygen limitation

“…() suggested that whether taxa show oxygen limitation at thermal extremes may be contingent on their capacity to regulate oxygen uptake, which in turn, could help explain differences in support for oxygen limitation between aquatic and terrestrial ectotherms. Indeed, studies on insects and freshwater snails indicate that the extent to which taxa show oxygen‐limited thermal tolerance depends on the ability of animals to regulate oxygen uptake (Boardman & Terblanche, ; Koopman et al., ; Verberk & Bilton, , ). All the species investigated in our study have similar gas exchange mechanisms (i.e.…”

Thermal limits to survival and activity in two life stages of false codling moth Thaumatotibia leucotreta (Lepidoptera, Tortricidae)

“…There are several possible mechanisms worthy of further consideration but perhaps most the important are the small HSPs and ion homeostasis (O'Sullivan et al ., ; Zhang et al ., ), as well as their potential interaction (Armstrong et al ., ), which are increasingly implicated in invertebrate heat tolerance. It remains unlikely that oxygen limitation plays a role in mechanistically governing CT min in larvae (Boardman et al ., ), although it would be useful to consider this hypothesis at high temperatures and across life stages, given that another moth species, Bombyx mori , show strongly divergent stage‐related responses (Boardman & Terblanche, ).…”

Promises and challenges in insect–plant interactions

“…For example, changing humidity or Figure 5 For insects living at the leaf surfacehere, a member of the Acrididae at the surface of a piper leaf in Ecuadorbiophysical mechanisms are at play to determine the body temperature of the insect and further its survival and performance. Indeed, this dovetails with a major research focus area for arthropod thermal physiologythe link between an organism's metabolic supply and demand and whether it sets thermal tolerance in a deterministic fashion (e.g., Boardman & Terblanche, 2015;reviewed in Verberk et al, 2016). These heat fluxes between the leaf surface and the environment determine directly the leaf temperature depending on the stomatal behaviour, and they also indirectly influence the plant's chemical defences, its nutritional quality, and the emission of volatile organic compounds (VOCs).…”

“…Another example: for insect-built structures such as galls or cambium mines, a change in gas composition within the structurefor instance, after a sudden variation in plant assimilation ratemight make the insect less tolerant to high temperatures (Pincebourde & Casas, 2016). Indeed, this dovetails with a major research focus area for arthropod thermal physiologythe link between an organism's metabolic supply and demand and whether it sets thermal tolerance in a deterministic fashion (e.g., Boardman & Terblanche, 2015;reviewed in Verberk et al, 2016).…”