Cockroaches That Exchange Respiratory Gases Discontinuously Survive Food and Water Restriction

Abstract

Metabolic rate and respiratory gas exchange patterns vary significantly both between and within species, even after a number of biotic and abiotic factors are taken into account. This suggests that such variation is of evolutionary importance, but the life history implications of this variation remain relatively poorly characterized. In the present study, we examine the effect of metabolic variation on starvation and desiccation resistance in the speckled cockroach Nauphoeta cinerea. We also compare the starvation and desiccation resistance of individuals that exchange respiratory gases continuously with those that breathe discontinuously.We show that metabolic rate has no effect on survival during food and water restriction, but cockroaches exhibiting discontinuous gas exchange cycles (DGCs) live longer than those that do not and those provisioned with water lived longer than those that were not. This finding represents the first demonstration that DGCs confer a fitness benefit, and supports the oldest hypothesis for the evolution of DGCs (which suggests that DGCs arose or are maintained to reduce respiratory water loss) as we also reveal reduced water loss (both respiratory and total) in cockroaches exhibiting discontinuous gas exchange. K E Y W O R D S :DGC, discontinuous, fitness, gas, metabolism, Nauphoeta cinerea.The rate at which organisms use energy for anabolic and catabolic reactions (metabolic rate) is known to vary widely both between and within species. Metabolic rate scales positively with body mass, and variation in mass accounts for the majority (>90%) of interspecific variation (Mueller and Diamond 2001;White et al. 2006;Chown et al. 2007). However, similarly sized species of ectotherm can show metabolic rates that differ by over an order of magnitude (White et al. 2006) and individuals of the same species can differ by up to a several fold (Speakman et al. 2004). It is now well known that metabolism is influenced by many biotic and abiotic factors such as age, sex, activity, thermoregulatory strategy, reproductive, and absorptive states as well as temperature and aridity (Mueller and Diamond 2001; Addo-Bediako et al.

Reversible brain inactivation induces discontinuous gas exchange in cockroaches

“…The protracted closure of spiracles during the DGC's C phase and intermittent opening during the F phase will reduce an insect's rate of respiratory water loss (e.g. Williams et al, 2010), and there is evidence that this confers increased fitness during periods of starvation and water restriction, at least in cockroaches Nauphoeta cinerea (Schimpf et al, 2012). Similarly, low tracheal O 2 levels during the C and F phases of the DGC have been observed in several species (Hetz and Bradley, 2005), and have been suggested to ameliorate toxic levels of oxygen free radicals when the insect's MR is low (Bradley, 2000).…”

“…However, the coincidence between inactivity, low metabolic rate and DGCs does not mean that it is low MR per se that drives the emergence of this pattern. Indeed, there is considerable overlap between the MRs of insects displaying DGCs and continuous gas exchange patterns Schimpf et al, 2012;Williams et al, 2010). While it is perhaps unsurprising that the respiratory requirements of a resting insect can be satisfied equally well by either a continuous or a discontinuous gas exchange pattern, it does raise the question: why change to a discontinuous pattern of gas exchange during periods of inactivity instead of regulating a low continuous rate of gas exchange?…”

Gas exchange patterns in Platynus assimilis (Coleoptera: Carabidae): Respiratory failure induced by a pyrethroid

“…Separate CO2 and O2 systems as a non-adaptive explanation for DGE behaviour does not contradict several adaptive explanations (Hetz & Bradley, 2005;Förster & Hetz, 2010;Chown et al, 2011). The lengthening of the C-phase and shortening of the O-phase restrict water loss (Schimpf et al, 2012). A very long C-phase, lasting nearly one day, is characteristic of diapausing pupae of the cabbage white butterfly, Pieris brassicae .…”

“…Thus, ceasing to breath by means of DGE is harmful for insects. According to Schimpf et al (2012) insects breathing by means of DGE survive for longer when deprived of food and water, which indicates that DGE confers a fitness benefit by reducing water loss.…”

The effect of discontinuous gas exchange on respiratory water loss in grasshoppers (Orthoptera: Acrididae) varies across an aridity gradient

“…For example, chronic exposure of cockroaches to low humidity results in shorter bursts of gas exchange, correlated with reduced rates of body mass loss (Schimpf et al, 2009). Employing DGC is also associated with increased desiccation and starvation resistance (Schimpf et al, 2012). Lower rates of RWL are associated with DGC compared with continuous exchange in lepidopteran larvae (Williams et al, 2010), but findings from similar studies are contradictory to predictions of the hygric hypothesis in ants (Gibbs and Johnson, 2004;Lighton et al, 2004;Lighton and Turner, 2008) and cockroaches (Groenewald et al, 2013).…”