Discontinuous gas exchange in the fire ant, Solenopsos invicta Buren:

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.

Section: Discussionsupporting

confidence: 86%

Section: Introductionmentioning

confidence: 99%

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

Terblanche

Clusella‐Trullas

Chown

2010

“…The presence of a critical P CO 2 threshold dictates that the amount of CO 2 released in a single respiratory burst, or spiracular open period, would remain constant as long as the threshold value does not change. However, many studies have demonstrated that the respiratory burst volume decreases with increased temperature in ants (Lighton, 1988;Quinlan and Lighton, 1999;Vogt and Appel, 2000), beetles (Duncan and Dickman, 2001) and the cecropia silkworm (Schneiderman and Williams, 1955). Others have found no change in burst volume with increasing temperature (Davis et al, 1999;Klok and Chown, 2005), or even an increase in burst volume (Shelton and Appel, 2001;Basson and Terblanche, 2011).…”

Section: Discussionmentioning

confidence: 99%

Temperature-dependent variation in gas exchange patterns and spiracular control in Rhodnius prolixus

Heinrich

Bradley

2014

Insects display an array of respiratory behaviors, including the use of discontinuous gas exchange. This pattern is characterized by periods of spiracular closure, micro-openings (flutter), and complete openings during which the majority of gas exchange takes place. A current model of insect spiracular control suggests that spiracles are controlled by two interacting feedback loops, which produce the discontinuous pattern. The flutter period is thought to be initiated by a critically low partial pressure of oxygen, while the open period is initiated by a critically high CO 2 threshold. The goal of our study was to test this control model under conditions of feeding-induced or temperature-induced changes in metabolic rate. We manipulated the metabolic rate of the insect Rhodnius prolixus using two discrete mechanisms: (1) feeding the insects a bloodmeal or (2) exposing them to a range of temperatures (18-38°C). Examining the variation in the gas exchange patterns produced by insects in each of these treatments allowed us to determine whether spiracular control is sensitive to metabolic rate and/or temperature. We found that increases in temperature caused significant decreases in open phase burst volumes and premature abandonment of discontinuous gas exchange cycles. These effects were not observed in fed individuals maintained at a single temperature despite their higher metabolic rates. Our results indicate that some part of the spiracular control mechanism is temperature sensitive, suggesting a possible role for pH in CO 2 sensing.

“…Similarly, in a comparative analysis of water balance in Drosophila species from mesic and xeric habitats, Gibbs et al (2003) concluded that lower rates of water loss in the xeric species are achieved primarily by reduction in respiratory losses associated with a reduction in metabolic rate and activity levels, and improved spiracular control. Based on investigations of discontinuous gas exchange in beetles, Duncan and Dickman (2001) and Duncan et al (2002a) supported the water conservation hypothesis for the DGC because the other hypotheses seemed not to apply to the species they investigated (see also Vogt and Appel, 2000). Indeed, Duncan (2003) went on to conclude that every facet of the DGC can be altered (presumably in an adaptive fashion) to effect respiratory water savings.…”

mentioning

confidence: 99%

Discontinuous gas exchange and the significance of respiratory water loss in scarabaeine beetles

Chown

Davis

2003

SUMMARYRespiratory water loss in insects is a controversial topic. Whilst earlier studies considered respiratory transpiration a significant component of overall water loss, to the extent that it was thought to be responsible not only for the evolution of discontinuous gas exchange cycles (DGCs) but also for variation in DGC patterns, later work repeatedly questioned its importance. In particular, investigations of the proportional contribution of respiratory transpiration to total water loss in species showing DGCs suggested that respiratory transpiration was unlikely to be important in these species. In turn, these studies have been criticized on analytical grounds. In this study we investigated variation in cuticular and respiratory water loss rates in five Scarabaeus dung beetle species, all of which show discontinuous gas exchange cycles, to ascertain the significance of respiratory water loss using modern analytical techniques. In particular, we determined whether there is variation in water loss rates amongst these beetles, whether both respiratory and cuticular water loss rates contribute significantly to variation in the former, and whether metabolic rate variation and variation in the duration of the DGC periods contribute significantly to variation in respiratory water loss rate. Total water loss rate varied such that species from arid areas had the lowest rates of water loss, and both cuticular and spiracular transpiration contributed significantly to variation in overall water loss rate. Moreover, variation in metabolic rate and in the duration of the DGC periods contributed significantly to variation in respiratory water loss rate. By contrast, examination of proportional water loss revealed little other than that it varies between 6.5% and 21%, depending on the species and the temperature at which it was examined. Cuticular water loss scaled as mass0.721, but did not differ from that expected from geometric considerations alone. By contrast, respiratory water loss scaled as mass0.531, suggesting that gas exchange takes place by diffusion and convection. Our results provide direct evidence that respiratory water loss forms a significant component of water balance, and that changes in both metabolic rate and DGC characteristics contribute to modulation of respiratory water loss.