Phenotypic plasticity of gas exchange pattern and water loss in Scarabaeus spretus (Coleoptera: Scarabaeidae): deconstructing the basis for metabolic rate variation

Abstract

SUMMARYInvestigation of gas exchange patterns and modulation of metabolism provide insight into metabolic control systems and evolution in diverse terrestrial environments. Variation in metabolic rate in response to environmental conditions has been explained largely in the context of two contrasting hypotheses, namely metabolic depression in response to stressful or resource-(e.g. water) limited conditions, or elevation of metabolism at low temperatures to sustain life in extreme conditions. To deconstruct the basis for metabolic rate changes in response to temperature variation, here we undertake a full factorial study investigating the longer-and short-term effects of temperature exposure on gas exchange patterns. We examined responses of traits of gas exchange [standard metabolic rate (SMR); discontinuous gas exchange (DGE) cycle frequency; cuticular, respiratory and total water loss rate ( -1 in 15°C-acclimated beetles to 3.1±0.5mgh -1 in 25°C-acclimated beetles measured at 25°C). Respiratory WLR was reduced from 2.25±0.40mgh -1 in 15°C-acclimated beetles to 1.60±0.40mgh -1 in 25°C-acclimated beetles measured at 25°C, suggesting conservation of water during DGE bursts. Overall, this suggests water conservation is a priority for S. spretus exposed to longer-term temperature variation, rather than elevation of SMR in response to low temperature acclimation, as might be expected from a beetle living in a relatively warm, low rainfall summer region. These results are significant for understanding the evolution of gas exchange patterns and trade-offs between metabolic rate and water balance in insects and other terrestrial arthropods.

Aquatic insects in a multistress environment: cross-tolerance to salinity and desiccation

“…The control of cuticle permeability is also one of the main mechanisms used to prevent water loss in terrestrial insects and has been shown to be a phenotypically plastic trait (e.g. Stinziano et al, 2015;Terblanche et al, 2010), although its role in aquatic insects has been less well explored (e.g. Alarie et al, 1998;Jacob and Hanssen, 1986).…”

Water loss in tree weta (Hemideina): adaptation to the montane environment and a test of the melanisation–desiccation resistance hypothesis

“…Most insects that remain active in desiccating environments do so by retaining water more effectively through a reduction in the rate of water loss (Gibbs and Matzkin, 2001). This is achieved through a combination of limiting excretory water losses through the mouthparts or anus (Bursell, 1960), by regulating diuresis by decreasing Malpighian tubule activity and/or increasing resorption in the hind-gut (Park, 2012), through reducing respiratory water loss (RWL) via changes in respiratory patterns (Chown et al, 2006;Marais et al, 2005;Terblanche et al, 2010) and through decreasing cuticular water loss (CWL) by reducing cuticular permeability (Chown and Nicolson, 2004).…”

Gas exchange patterns and water loss rates in the Table Mountain cockroach,Aptera fusca(Blattodea: Blaberidae)

“…Schimpf et al, 2009;Williams et al, 2010) or metabolic rate modulation (e.g. Terblanche et al, 2010), particularly under xeric conditions (e.g. Gefen, 2011), and may therefore be linked to evolutionary fitness (e.g.…”

“…Schimpf et al, 2012). Manipulation of environmental conditions (such as temperature, moisture or oxygen availability) or the insect's state (rest versus active, dehydrated versus hydrated) can have a dramatic influence on the pattern and overall flux rates exhibited (see Lighton and Turner, 2008;Schimpf et al, 2009;Terblanche et al, 2008;Terblanche et al, 2010;Williams et al, 2010;Matthews and White, 2011a;Matthews and White, 2011b).…”

“…One of the most prominent, and perhaps well supported, is the hygric hypothesis, which states that DGE evolved to reduce RWL by extending the C phase or reducing the O phase (Kestler, 1985;Lighton, 1994;Chown, 2002;Duncan et al, 2002;Chown and Davis, 2003;Chown et al, 2006b;White et al, 2007;Schimpf et al, 2009;Terblanche et al, 2010;Williams et al, 2010;Chown, 2011). However, this notion is not without controversy (see discussions in Chown, 2011;Contreras and Bradley, 2011;Matthews and White, 2011a), at least partly owing to the mechanisms by which RWL and CWL are regulated, their relative contribution to total water loss (TWL) (Chown, 2002;Chown and Davis, 2003;Terblanche et al, 2010) and the fact that many insects abandon DGE under conditions when it is thought to be most useful for water saving [e.g. higher temperatures, dehydration ].…”