Intra-individual variation allows an explicit test of the hygric hypothesis for discontinuous gas exchange in insects

Biology Letters, Apr 2010

The hygric hypothesis postulates that insect discontinuous gas exchange cycles (DGCs) are an adaptation that reduces respiratory water loss (RWL), but evidence is lacking for reduction of water loss by insects expressing DGCs under normal ecological conditions. Larvae of Erynnis propertius (Lepidoptera: Hesperiidae) naturally switch between DGCs and continuous gas exchange (CGE), allowing flow-through respirometry comparisons of water loss between the two modes. Water loss was lower during DGCs than CGE, both between individuals using different patterns and within individuals using both patterns. The hygric cost of gas exchange (water loss associated with carbon dioxide release) and the contribution of respiratory to total water loss were lower during DGCs. Metabolic rate did not differ between DGCs and CGE. Thus, DGCs reduce RWL in E. propertius, which is consistent with the suggestion that water loss reduction could account for the evolutionary origin and/or maintenance of DGCs in insects.

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Intra-individual variation allows an explicit test of the hygric hypothesis for discontinuous gas exchange in insects

Caroline M. Williams Shannon L. Pelini Jessica J. Hellmann Brent J. Sinclair Articles on similar topics can be found in the following collections Receive free email alerts when new articles cite this article - sign up in the box at the top right-hand corner of the article or click here References Subject collections Email alerting service Intra-individual variation allows an explicit test of the hygric hypothesis for discontinuous gas exchange in insects Caroline M. Williams1, Shannon L. Pelini2,, Jessica J. Hellmann2 and Brent J. Sinclair1,* 1Department of Biology, University of Western Ontario, London, ON N6A 5B7, Canada 2Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556, USA *Author for correspondence (). Present address: Harvard Forest, Harvard University, Petersham, MA 01366, USA The hygric hypothesis postulates that insect discontinuous gas exchange cycles (DGCs) are an adaptation that reduces respiratory water loss (RWL), but evidence is lacking for reduction of water loss by insects expressing DGCs under normal ecological conditions. Larvae of Erynnis propertius (Lepidoptera: Hesperiidae) naturally switch between DGCs and continuous gas exchange (CGE), allowing flow-through respirometry comparisons of water loss between the two modes. Water loss was lower during DGCs than CGE, both between individuals using different patterns and within individuals using both patterns. The hygric cost of gas exchange (water loss associated with carbon dioxide release) and the contribution of respiratory to total water loss were lower during DGCs. Metabolic rate did not differ between DGCs and CGE. Thus, DGCs reduce RWL in E. propertius, which is consistent with the suggestion that water loss reduction could account for the evolutionary origin and/or maintenance of DGCs in insects. 1. INTRODUCTION Discontinuous gas exchange cycles (DGCs) have evolved independently at least five times in insects (Marais et al. 2005). The evolutionary pressures that lead to DGCs are debated (Chown et al. 2006). DGCs consist of three phases: closed phase during which spiracles are closed and there is no external gas exchange; flutter phase where spiracles rapidly open and close, allowing bulk inflow of air, and open phase where spiracles are open to allow unrestricted gas exchange (Chown et al. 2006). Three main adaptive hypotheses have been proposed to explain the origin and maintenance of DGCs (Chown et al. 2006). The hygric hypothesis contends that DGCs have evolved to limit respiratory Electronic supplementary material is available at http://dx.doi.org/ 10.1098/rsbl.2009.0803 or via http://rsbl.royalsocietypublishing.org. water loss (RWL) by maximizing the time that the spiracles are closed, and minimizing water efflux due to bulk inward convection in the F-phase (Chown et al. 2006). The chthonic hygric hypothesis (Lighton & Berrigan 1995) states that DGCs originated in insects inhabiting hypoxic and hypercapnic (primarily underground) environments to increase O2 and CO2 diffusion gradients, with coincidental water savings. The oxidative damage hypothesis (Hetz & Bradley 2005) suggests that DGCs minimize oxidative damage during periods of low metabolic demand, by maintaining low tracheal PO2 while retaining delivery capacity during periods of high metabolic demand (e.g. flight). Here, we focus on the water retention benefits of DGCs, primarily addressing the hygric hypothesis. We note the difficulty in distinguishing the hygric and chthonic hygric hypotheses based on water loss, but the hygric hypothesis may be rejected independently of the chthonic and oxidative damage hypotheses since CO2 and O2 partial pressures are central to the latter (Chown et al. 2006). The hygric hypothesis predicts that (i) water lost per CO2 released will be lower for insects using DGCs (see also Lighton & Turner 2008) and (ii) DGCs will decrease RWL. Measurement of water loss within DGCs shows that RWL is greater when the spiracles are open (see Chown 2002). DGCs are longer in species from xeric environments (White et al. 2007), while cyclic and continuous patterns are more prevalent in mesic habitats (Marais et al. 2005). RWL was lower in individual ants that did not express DGCs; however, those individuals also had lower metabolic rates (Gibbs & Johnson 2004). Manipulation of environmental variables can force insects to abandon DGCs (e.g. Lighton & Turner 2008; Terblanche et al. 2008), but to our knowledge there have been no comparisons of RWL in individuals that use both DGCs and continuous gas exchange (CGE) under ecologically relevant conditions. Erynnis propertius (Lepidoptera: Hesperiidae) overwinter as quiescent late-instar larvae in rolls of dry oak leaves (Prior et al. 2009). Quiescent larvae probably experience desiccation during the overwintering period as no feeding occurs. Under benign conditions, individuals use both DGCs and CGE, allowing a direct comparison of water loss rates both between an (...truncated)


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Caroline M. Williams, Shannon L. Pelini, Jessica J. Hellmann, Brent J. Sinclair. Intra-individual variation allows an explicit test of the hygric hypothesis for discontinuous gas exchange in insects, Biology Letters, 2010, pp. 274-277, 6/2, DOI: 10.1098/rsbl.2009.0803