Discontinuous respiration in insects—II. The direct measurement and significance of changes in tracheal gas composition during the respiratory cycle of silkworm pupae

Levy, Robert I.; Schneiderman, Howard A.

doi:10.1016/0022-1910(66)90068-0

Cited by 155 publications

(96 citation statements)

References 18 publications

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“…During DGCs, external openings of the tracheal system, the spiracles, are sealed shut for extended periods punctuated by brief openings (39). During the closed phase, CO 2 , which is far more soluble than oxygen (26), is forced into the body fluids (40,41). However, maintaining acid-base homeostasis over time scales longer than individual ventilation cycles requires that insects rid themselves of essentially as much CO 2 as they consume O 2 .…”

Section: Discussionmentioning

confidence: 99%

Universal model for water costs of gas exchange by animals and plants

Woods

Smith

2010

Proc. Natl. Acad. Sci. U.S.A.

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For terrestrial animals and plants, a fundamental cost of living is water vapor lost to the atmosphere during exchange of metabolic gases. Here, by bringing together previously developed models for specific taxa, we integrate properties common to all terrestrial gas exchangers into a universal model of water loss. The model predicts that water loss scales to gas exchange with an exponent of 1 and that the amount of water lost per unit of gas exchanged depends on several factors: the surface temperature of the respiratory system near the outside of the organism, the gas consumed (oxygen or carbon dioxide), the steepness of the gradients for gas and vapor, and the transport mode (convective or diffusive). Model predictions were largely confirmed by data on 202 species in five taxa-insects, birds, bird eggs, mammals, and plants-spanning nine orders of magnitude in rate of gas exchange. Discrepancies between model predictions and data seemed to arise from biologically interesting violations of model assumptions, which emphasizes how poorly we understand gas exchange in some taxa. The universal model provides a unified conceptual framework for analyzing exchangeassociated water losses across taxa with radically different metabolic and exchange systems.ll terrestrial animals and plants exchange O 2 and CO 2 with the atmosphere and thereby incur costs in the currency of water vapor (1-4). The inevitability of water loss stems from universal characteristics of terrestriality-(i) adequate gas exchange requires large surface areas of high-conductance tissues, usually invaginated; (ii) high-conductance tissues saturate internal exchange spaces with water vapor; and (iii) those surfaces must be ventilated by the atmosphere, at least intermittently. Consequently, water vapor tends to escape into surrounding drier air. Terrestrial organisms-here defined to include air-breathing marine mammals-thus face a gas-water tradeoff in which higher rates of gas exchange give higher rates of water loss. For individual organisms, this tradeoff shapes patterns of ventilation and behavior. For populations and species, the tradeoff influences diverse phenomena, including the evolution of hibernation, dormancy, and diapause (5-8), the evolution of nasal physiology in vertebrate homeotherms (9-11), and the evolution and ecology of plants with different modes of carbon fixation (C3, C4, and CAM) (12). In general, the severity of the tradeoff for any species will depend on the fraction of total water lost through the gas-exchange system, which in turn is related to the temperature and aridity of its habitat (13).The diversity of gas-exchange systems among taxa has spawned a large set of models for predicting respiratory and stomatal water losses (14-21). Although the models are all quite similar, they have failed to provide unification and generality as a group, because each uses different terminology and is built on taxonspecific details. Broader conceptualization of the problem may give insight into how diverse organisms function across biome...

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Section: Discussionmentioning

confidence: 99%

Universal model for water costs of gas exchange by animals and plants

Woods

Smith

2010

Proc. Natl. Acad. Sci. U.S.A.

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“…Between 1953 and 1974, Schneiderman and his colleagues published a number of elegant studies on the discontinuous respiration cycles of Cecropia silkworms (see for example, Schneiderman & Williams, 1955;Levy & Schneiderman, 1958, 1966aSchneiderman, 1956Schneiderman, , 1960Schneiderman & Schechter, 1966;Brockway & Schneiderman, 1967;Burkett & Schneiderman, 1974a, b). Indoctrinated by the diffusion theory of Krogh (1920), they believed at that time that the pupae of Cecropia could easily satisfy their respiratory demands by passive diffusion of O2 and CO2 through the spiracles, without the necessity of ventilatory movements.…”

Section: Discussionmentioning

confidence: 99%

“…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). The high concentration of CO2 then caused the spiracular valves to open and let the accumulated CO2 diffuse out through the widely open spiracles (see reviews by Buck, 1962;Brockway & Schneiderman, 1967;Burkett & Schneiderman, 1974b;Miller, 1981;Kestler, 1985;Lighton, 1996;Wasserthal, 1996).…”

Section: Introductionmentioning

confidence: 99%

“…In their original observations on discontinuous respiration cycles in Cecropia, Schneiderman and his co-workers also denied the presence of active respiratory movements, except those of the spiracular valves (Levy & Schneiderman, 1966a). They found that the valves of the abdominal spiracles occasionally "fluttered" 16-to 22-times per min.…”

Section: Introductionmentioning

confidence: 99%

“…They found that the valves of the abdominal spiracles occasionally "fluttered" 16-to 22-times per min. The spiracular "fluttering" was observed and described many times (Schneiderman, 1956(Schneiderman, , 1960Levy & Schneiderman, 1958, 1966a and evidence of it was also present in graphical recordings (Schneiderman, 1960). However, its physiological function was never sufficiently explained.…”

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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