Discontinuous gas exchange in insects

Quinlan, Michael; Gibbs, Allen G.

doi:10.1016/j.resp.2006.04.004

Cited by 76 publications

(85 citation statements)

References 74 publications

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“…Even in diapausing Cecropia, the feature is limited to CO2 bursts or may be absent. Obviously, these results conflict with the standard interpretation of discontinuous respiration cycles (DGC), which traditionally place the periods of "fluttering" where they can never occur (Lighton, 1996;Quinlan & Gibbs, 2006). …”

Section: Fluttering Spiracles and Extracardiac Pulsationsmentioning

confidence: 69%

“…Termites, for example, exhale volumes of CO2 that are greater than the volume of their whole body (Sláma, et al 2007) within periods of less than one minute. Most respirometric investigations are based on IR-flow-through, direct recordings of CO2 output (for reviews see Lighton, 1996;Quinlan & Gibbs, 2006;Chown et al, 2006). Unfortunately, flow-through techniques are unable to distinquish between the CO2 produced by simple diffusion and the chemical release of gaseous CO2 from carbonate buffers.…”

Section: Open Spiracles and The Co2 Burstsmentioning

confidence: 99%

“…Accordingly, these discontinuous respiration cycles were assumed to be caused by the mechanical opening or closing of the spiracular valves triggered by the composition of intratracheal gas (Schneiderman, 1960;Schneiderman & Schechter, 1966;Levy & Schneiderman, 1966a, b, c;Brockway & Schneiderman, 1967). Krogh's illusive concept led Schneiderman and his co-workers (see Schneiderman, 1960;Levy & Schneiderman, 1966a, b, c) to develop a theory of stereotypic, 3-phasic DGC (discontinuous gas cycles) or OCF cycles (O for open, C for closed and F for fluttering spiracles) by later authors (Kestler, 1985;Lighton, 1996;Chown et al, 2006;Quinlan & Gibbs, 2006). According to these mechanistic DGC or OCF concepts, gaseous CO2 should continuously accumulate within the closed tracheal system until its concentration reached about 6.4% (Levy & Schneiderman, 1958, 1966aSchneiderman, 1960).…”

Section: Introductionmentioning

confidence: 99%

“…More recent reviews on the discontinuous respiration of insects (for references see Chown et al, 2006;Quinlan & Gibbs, 2006;Contreras & Bradley, 2009) still adhere fully to the mechanistic, 85-year-old diffusion theory of Krogh (1920). They completely ignore the existence of ventilatory movements, neglect the programmed nervous operation of the spiracular valves (note that internal gas concentrations change within intervals of many minutes, while spiracular valves open and close in milliseconds) and claim that the discontinuous bursts of CO2 are only due to the passive, physical diffusion of the accumulated CO2 through open spiracles.…”

Section: Introductionmentioning

confidence: 99%

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A new look at discontinuous respiration in pupae of Hyalophora cecropia (Lepidoptera: Saturniidae): Haemocoelic pressure, extracardiac pulsations and O<sub>2 </sub>consumption

Sláma¹

2010

Eur. J. Entomol.

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Abstract. Discontinuous respiration in diapausing pupae of Cecropia silkworms was monitored by means of several electronic methods, including recording changes in haemocoelic pressure, monitoring respiratory movements by strain-gauge sensors and nanorespirographic recording of O2 consumption and CO2 output. It appears that, in contrast to previous concepts of stereotypic discontinuous respiration cycles (DGC) driven by accumulation of gaseous CO2 in the body, the new results indicate that CO2 remains dissolved in liquid carbonate buffers during interburst periods. In other words, there is no accumulation of gaseous CO2 within the air filled tracheal space between the bursts. The bursts of CO2 are caused by homeostatically regulated enzymatic hydration by carbonic anhydrase of metabolically produced carbonic acid. The chemically produced gaseous CO2 was exhaled mainly by a bulk outflow through selectively opened or pulsating spiracles. The output of CO2 was enhanced by actively regulated, unidirectional ventilation. The deep depressions in haemocoelic pressure, caused by permanent closure of all spiracular valves for long periods, appeared to be a specific feature of diapausing saturniid pupae. Physiologically, it has circulatory, not respiratory functions. The original definition of spiracular "fluttering" resulted from a misinterpretation of previously unknown extracardiac pulsations in haemocoelic pressure. The coordinated pulsation of the spiracular valves with extracardiac pulsations produce a very efficient, unidirectional ventilation of the whole tracheal system. According to the new results, the discontinuous respiration cycles of diapausing Cecropia pupae can be briefly described as follows: (1) Spiracular valves are kept permanently closed during the periods of deep depressions, they remain closed for some 99% of the time with occasional snap opening (passive inspirations) during prolonged interburst periods and more than 50% closed during the bursts; (2) During the long interburst periods, CO2 is retained in liquid carbonate buffers, while the relatively high (after the burst) or low (toward the next burst) rate of O2 consumption creates an internal vacuum, which is homeostatically compensated for by the snap-opening of one or just a few spiracular valves (passive suction inspirations); (3) The CO2 gas, produced enzymatically by carbonic anhydrase, enters the air filled tracheal system and leaves the body by diffusion, a bulk outflow, or actively regulated unidirectional ventilation ("fluttering" spiracles). The selective advantage of this actively regulated respiratory system for water retention in pupae is discussed. 487* This work is dedicated to the memory of the late Prof. H.A. Schneiderman for his pioneering work on discontinuous respiration cycles in insects. Prof. Schneiderman was awarded the Gregor Mendel gold medal by the Czechoslovak Academy of Sciences in 1990. His extensive reprint collection on insect respiration was kindly donated to the Institute of Entomology, Czech Academy of Sciences...

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Section: Fluttering Spiracles and Extracardiac Pulsationsmentioning

confidence: 69%

Section: Open Spiracles and The Co2 Burstsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A new look at discontinuous respiration in pupae of Hyalophora cecropia (Lepidoptera: Saturniidae): Haemocoelic pressure, extracardiac pulsations and O<sub>2 </sub>consumption

Sláma¹

2010

Eur. J. Entomol.

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“…Many toxic substances are able to evoke respiratory failure in insects (reviewed in Kuusik et al, 2001a;Jõgar et al, 2005;Karise and Mänd, 2015). DGE, in which CO 2 is released periodically as bursts, is a common respiratory pattern in many insects (reviewed in Lighton, 1994Lighton, , 1996Chown and Nicolson, 2004;Quinlan and Gibbs, 2006). The DGE cycle has three consecutive phases, the open or O-phase, the facultative closure or C-phase and the flutter or F-phase.…”

Section: Introductionmentioning

confidence: 99%

The opening-closing rhythms of the subelytral cavity associated with gas exchange patterns in diapausing Colorado potato beetle, Leptinotarsa decemlineata

Kuusik

Jõgar

Metspalu

et al. 2016

Journal of Experimental Biology

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The opening-closing rhythms of the subelytral cavity and associated gas exchange patterns were monitored in diapausing Leptinotarsa decemlineata beetles. Measurements were made by means of a flowthrough CO 2 analyser and a coulometric respirometer. Under the elytra of these beetles there is a more or less tightly enclosed space, the subelytral cavity (SEC). When the cavity was tightly closed, air pressure inside was sub-atmospheric, as a result of oxygen uptake into the tracheae by the beetle. In about half of the beetles, regular opening-closing rhythms of the SEC were observed visually and also recorded; these beetles displayed a discontinuous gas exchange pattern. The SEC opened at the start of the CO 2 burst and was immediately closed. On opening, a rapid passive suction inflow of atmospheric air into the SEC occurred, recorded coulometrically as a sharp upward peak. As the CO 2 burst lasted beyond the closure of the SEC, we suggest that most of the CO 2 was expelled through the mesothoracic spiracles. In the remaining beetles, the SEC was continually semi-open, and cyclic gas exchange was exhibited. The locking mechanisms and structures between the elytra and between the elytra and the body were examined under a stereomicroscope and by means of microphotography. We conclude that at least some of the L. decemlineata diapausing beetles were able to close their subelytral cavity tightly, and that the cavity then served as a water-saving device.

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2011

Ecology and Evolution of Dung Beetles

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Discontinuous gas exchange in insects

Cited by 76 publications

References 74 publications

A new look at discontinuous respiration in pupae of Hyalophora cecropia (Lepidoptera: Saturniidae): Haemocoelic pressure, extracardiac pulsations and O<sub>2 </sub>consumption

A new look at discontinuous respiration in pupae of Hyalophora cecropia (Lepidoptera: Saturniidae): Haemocoelic pressure, extracardiac pulsations and O<sub>2 </sub>consumption

The opening-closing rhythms of the subelytral cavity associated with gas exchange patterns in diapausing Colorado potato beetle, Leptinotarsa decemlineata

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