Discontinuous Gas Exchange in Insects: A Clarification of Hypotheses and Approaches (original) (raw)
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Evolutionary responses of discontinuous gas exchange in insects
Proceedings of the National Academy of Sciences, 2007
The discontinuous gas-exchange cycles (DGCs) observed in many quiescent insects have been a cause of debate for decades, but no consensus on their evolutionary origin or adaptive significance has been achieved. Nevertheless, three main adaptive hypotheses have emerged: (i) the hygric hypothesis suggests that DGCs reduce respiratory water loss; (ii) the chthonic hypothesis suggests that DGCs facilitate gas exchange during environmental hypoxia, hypercapnia, or both; and (iii) the oxidative-damage hypothesis suggests that DGCs minimize oxidative tissue damage. However, most work conducted to date has been based on single-species investigations or nonphylogenetic comparative analyses of few species, despite calls for a strong-inference, phylogenetic approach. Here, we adopt such an approach by using 76 measurements of 40 wild-caught species to examine macrophysiological variation in DGC duration in insects. Potential patterns of trait variation are first identified on the basis of the explicit a priori predictions of each hypothesis, and the best phylogenetic generalized least-squares fit of the candidate models to the data is selected on the basis of Akaike's information criterion. We find a significant positive relationship between DGC duration and habitat temperature and an important interaction between habitat temperature and precipitation. This result supports the hygric hypothesis. We conclude that the DGCs of insects reduce respiratory water loss while ensuring adequate gas exchange.
Metabolic rates and water loss data from insects exhibiting discontinuous gas exchange
2021
The earliest description of the discontinuous gas exchange cycle (DGC) in lepidopterous insects supported the role played by the spiracles and tracheal system in modulating the release of carbon dioxide. Further understanding led to the idea that the adaptive significance of regulated opening and closure of the spiracles is to reduce water loss (hygric hypothesis) and facilitate gaseous exchange in hyperoxia/hypoxia (chthonic hypothesis). With technological advances, other insect orders were investigated and the hygric and chthonic hypotheses were questioned. To allow for broad-scale comparison and conclusion, we conducted a meta-analysis to evaluate the merit of both postulated hypotheses that included 46 insect species in 24 families across nine orders. We also quantified the percent change in metabolic rates per ºC change of temperature during DGC. DGC was shown to reduce water loss (-3.27 ± 0.88; estimate ± 95% confidence limits [95% CI]; <i>P</i> < 0.0001) in ins...
Discontinuous gas exchange and the significance of respiratory water loss in scarabaeine beetles
Journal of Experimental Biology, 2003
The significance of the contribution of respiratory transpiration to total water loss in insects is controversial. Early studies not only suggested that respiratory water loss forms an important component of total transpiration (Loveridge, 1968; Edney, 1977), but also argued that the need for reduction of respiratory transpiration has been a major factor underlying the evolution of discontinuous gas exchange (Levy and Schneiderman, 1966; Burkett and Schneiderman, 1974; Lighton, 1994). Discontinuous gas exchange cycles (DGCs) are usually confined to times when insects (or other arthropods; see Lighton, 1998; Klok et al., 2002) are at rest, and involve the alteration of three major periods: a Closed (C) period, during which the spiracles are tightly shut and there is no respiratory water loss, a Flutter (F) period, when convective flow of air into the tracheal system is thought to reduce water loss, and an Open (O) period, during which most water loss takes place because the spiracles are held open (Lighton, 1994, 1996). Because respiratory transpiration is mostly restricted to a short O-period, it has long seemed obvious that discontinuous gas exchange has evolved to reduce water loss (for reviews see Kestler, 1985; Lighton, 1994, 1996). Moreover, several studies have reported considerable variation in the characteristics (especially the duration) of the C-, F-and O-periods among species from different habitats, suggesting that modulating the characteristics of the periods is a significant way in which respiratory water loss might be altered (
Journal of Experimental Biology, 2004
Partitioning the relative contributions of cuticular and respiratory water loss in a tracheate arthropod is relatively easy if it undergoes discontinuous gas exchange cycles or DGCs, leaving its rate of cuticular water loss in primary evidence while its spiracles are closed. Many arthropods are not so obliging and emit CO 2 continuously, making cuticular and respiratory water losses difficult or impossible to partition. We report here that by switching ambient air from 21 to 100% O 2 , marked spiracular constriction takes place, causing a transient but substantial -up to 90% -reduction in CO 2 output. A reduction in water loss rate occurs at the same time. Using this approach, we investigated respiratory water loss in Drosophila melanogaster and in two ant species, Forelius mccooki and Pogonomyrmex californicus. Our resultsrespiratory water loss estimates of 23%, 7.6% and 5.6% of total water loss rates, respectively -are reasonable in light of literature estimates, and suggest that the 'hyperoxic switch' may allow straightforward estimation of respiratory water loss rates in arthropods lacking discontinuous gas exchange. In P. californicus, which we were able to measure with and without a DGC, presence or absence of a DGC did not affect respiratory vs total water loss rates.
Insects
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 spe...
Gas exchange patterns and water loss rates in the Table Mountain Cockroach (Aptera fusca)
Gas exchange and water loss in A. fusca 2 SUMMARY 16 The importance of metabolic rate and/or spiracle modulation for saving respiratory 17 water is contentious. One major explanation for gas exchange pattern variation in 18 terrestrial insects is to effect a respiratory water loss (RWL) saving. To test this, we 19 measured V . CO 2 and V . H 2 O in a previously unstudied, mesic cockroach, Aptera fusca, 20 and compared gas exchange and water loss parameters among the major gas 21 exchange patterns (continuous, cyclic, discontinuous gas exchange (DGE)) at a range 22 of temperatures. Mean V . CO 2 , V . H 2 O, and V . H 2 O per unit V . CO 2 did not differ among the 23 gas exchange patterns at all temperatures (p>0.09). There was no significant 24 association between temperature and gas exchange pattern type (p=0.63). Percentage 25 of RWL (relative to total water loss) was typically low (9.79±1.84%) and did not differ 26 significantly among gas exchange patterns at 15°C (p=0.26). The method of estimation 27 had a large impact on the %RWL and of three techniques investigated (traditional, 28 regression, hyperoxic switch), the traditional method generally performed best. In 29 many respects, A. fusca has typical gas exchange for what might be expected from 30 other insects studied to date (e.g. V . CO 2 , V . H 2 O, RWL and CWL). However, we found 31 for A. fusca that V . H 2 O expressed as a function of metabolic rate was significantly 32 higher than the expected consensus relationship for insects, suggesting it is under 33 considerable pressure to save water. Despite this, we found no consistent evidence 34 supporting the conclusion that transitions in pattern type yield reductions in RWL in 35 this mesic cockroach. 36 37 Key words: water conservation, hyperoxic switch method, regression method, metabolic 38 rates, metabolic efficiency. 39 40 The Journal of Experimental Biology -ACCEPTED AUTHOR MANUSCRIPT Gas exchange and water loss in A. fusca 61 associated CO 2 emission patterns: the open (O) spiracle phase, when gas exchange takes place 62 freely through diffusion (although sometimes aided by active convection (e.g. Loveridge, 63 1968; Miller, 1973; Groenewald et al., 2012)); the closed (C) spiracle phase, when there is no 64 exchange of gas between the insect's tracheae and the outside environment; and the flutter (F) 65 phase, when spiracles open and close rapidly and some exchange of gases occurs (e.g.