Why Do Insects Close Their Spiracles? A Meta-Analytic Evaluation of the Adaptive Hypothesis of Discontinuous Gas Exchange in Insects

SIMPLE SUMMARY: Insects breathe with the aid of thin capillary tubes that open out to the exterior of their body as spiracles. These spiracles are often modulated in a rhythmic gas pattern known as the discontinuous gas exchange cycle. During this cycle, spiracles are either firmly shut to allow no gaseous exchange or slightly open/fully open to allow for gaseous exchange. Two explanations are put forward to rationalize this process, namely, the rhythmic pattern is to (1) reduce water loss or (2) facilitate gaseous exchange in environments with high carbon dioxide and low oxygen. Interestingly, certain insects (such as some desert insects) do not use this rhythmic pattern where it would have been most beneficial and logical. Such an observation has led to the questioning of the explanations of the discontinuous gas exchange cycle. Consequently, we attempt to resolve this controversy by conducting a meta-analysis by synthesizing apposite data from across all insects where a discontinuous gas exchange cycle has been reported. A meta-analysis allows for a shift from viewing data through the lens of a single species to an order view. Thus, our goal is to use this holistic view of data to examine the explanations of the discontinuous gas exchange cycle across multiple groups of insects. ABSTRACT: The earliest description of the discontinuous gas exchange cycle (DGC) in lepidopterous insects supported the hypothesis that the DGC serves to reduce water loss (hygric hypothesis) and facilitate gaseous exchange in hyperoxia/hypoxia (chthonic hypothesis). With technological advances, other insect orders were investigated, and both hypotheses were questioned. Thus, we conducted a meta-analysis to evaluate the merit of both hypotheses. This included 46 insect species in 24 families across nine orders. We also quantified the percent change in metabolic rates per °C change of temperature during the DGC. The DGC reduced water loss (−3.27 ± 0.88; estimate ± 95% confidence limits [95% CI]; p < 0.0001) in insects. However, the DGC does not favor gaseous exchange in hyperoxia (0.21 ± 0.25 [estimate ± 95% CI]; p = 0.12) nor hypoxia, but did favor gaseous exchange in normoxia (0.27 ± 0.26 [estimate ± 95% CI]; p = 0.04). After accounting for variation associated with order, family, and species, a phylogenetic model reflected that metabolic rate exhibited a significant, non-zero increase of 8.13% (± 3.48 95% CI; p < 0.0001) per °C increase in temperature. These data represent the first meta-analytic attempt to resolve the controversies surrounding the merit of adaptive hypotheses in insects.