Hypoxia and hypercarbia in endophagous insects: Larval position in the plant gas exchange network is key

• A gas exchange framework was developed for miners, gallers and borers.
• Risks of hypoxia and hypercarbia are higher in galls than in mines in general.
• Cambium miners and borers are exposed to hypoxia and hypercarbia.
• Temperature and ambient CO2 alter gas diffusion pathways interactively.
• The eco-physiology of endophagous insects is still understudied.

Gas composition is an important component of any micro-environment. Insects, as the vast majority of living organisms, depend on O2 and CO2 concentrations in the air they breathe. Low O2 (hypoxia), and high CO2 (hypercarbia) levels can have a dramatic effect. For phytophagous insects that live within plant tissues (endophagous lifestyle), gas is exchanged between ambient air and the atmosphere within the insect habitat. The insect larva contributes to the modification of this environment by expiring CO2. Yet, knowledge on the gas exchange network in endophagous insects remains sparse. Our study identified mechanisms that modulate gas composition in the habitat of endophagous insects. Our aim was to show that the mere position of the insect larva within plant tissues could be used as a proxy for estimating risk of occurrence of hypoxia and hypercarbia, despite the widely diverse life history traits of these organisms. We developed a conceptual framework for a gas diffusion network determining gas composition in endophagous insect habitats. We applied this framework to mines, galls and insect tunnels (borers) by integrating the numerous obstacles along O2 and CO2 pathways. The nature and the direction of gas transfers depended on the physical structure of the insect habitat, the photosynthesis activity as well as stomatal behavior in plant tissues. We identified the insect larva position within the gas diffusion network as a predictor of risk exposure to hypoxia and hypercarbia. We ranked endophagous insect habitats in terms of risk of exposure to hypoxia and/or hypercarbia, from the more to the less risky as cambium mines > borer tunnels ≫ galls > bark mines > mines in aquatic plants > upper and lower surface mines. Furthermore, we showed that the photosynthetically active tissues likely assimilate larval CO2 produced. In addition, temperature of the microhabitat and atmospheric CO2 alter gas composition in the insect habitat. We predict that (i) hypoxia indirectly favors the evolution of cold-tolerant gallers, which do not perform well at high temperatures, and (ii) normoxia (ambient O2 level) in mines allows miners to develop at high temperatures. Little is known, however, about physiological and morphological adaptations to hypoxia and hypercarbia in endophagous insects. Endophagy strongly constrains the diffusion processes with cascading consequences on the evolutionary ecology of endophagous insects.

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