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Discontinuous Gas Exchange in Insects: Is It All in Their Heads? Author(S): Philip G

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Discontinuous Gas Exchange in Insects: Is It All in Their Heads? Author(S): Philip G The University of Chicago Discontinuous Gas Exchange in Insects: Is It All in Their Heads? Author(s): Philip G. D. Matthews and Craig R. White Source: The American Naturalist, Vol. 177, No. 1 (January 2011), pp. 130-134 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/10.1086/657619 . Accessed: 06/10/2015 21:47 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press, The American Society of Naturalists, The University of Chicago are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org This content downloaded from 23.235.32.0 on Tue, 6 Oct 2015 21:47:02 PM All use subject to JSTOR Terms and Conditions vol. 177, no. 1 the american naturalist january 2011 Notes and Comments Discontinuous Gas Exchange in Insects: Is It All in Their Heads? Philip G. D. Matthews* and Craig R. White School of Biological Sciences, University of Queensland, St. Lucia, Queensland 4072, Australia Submitted June 4, 2010; Accepted September 27, 2010; Electronically published November 18, 2010 exchange cycle (DGC) is perhaps the best known, most abstract: Some insects display an intermittent pattern of gas ex- intensively researched, and most vigorously debated of change while at rest, often going hours between breaths. These dis- continuous gas exchange cycles (DGCs) are known to have evolved these respiratory patterns (Chown et al. 2006). The typical independently within five insect orders, but their possible adaptive DGC is characterized by a period of negligible gas exchange benefit and evolutionary origin remain an enigma. Current research with the atmosphere when the spiracles are tightly shut is primarily concerned with testing three adaptive hypotheses: that (closed phase) followed by a period of intermittent carbon DGCs originally evolved or are currently maintained to (1) limit dioxide release and oxygen uptake as the insect’s spiracles respiratory water loss, (2) enhance gas exchange in subterranean “flutter” open and shut (flutter phase), which is terminated environments, or (3) limit oxidative damage. These adaptive expla- when the spiracles open fully, releasing a burst of carbon nations fail to unite a range of apparently contradictory observations dioxide while oxygen freely enters the tracheal system regarding the insects that display DGCs and the conditions under (open phase). While this respiratory pattern is described which they occur. Here we argue that DGCs are explained by cir- cadian, developmental, or artificially induced reductions in brain in most biology textbooks (e.g., Schmidt-Nielsen 1997), it activity. We conclude that this pattern results from the thoracic and is far from ubiquitous among insects. In fact, it is a pattern abdominal ganglia regulating ventilation in the absence of control that is known to occur among only a few insect orders from higher neural centers, and it is indicative of a sleeplike state. (ants, bees and wasps, butterflies and moths, beetles, grass- hoppers, and cockroaches; Marais et al. 2005) and then Keywords: DGC (discontinuous gas exchange cycle), periodic ven- only while at rest or during diapause as a pupa. Most tilation, brain, evolution, sleep, insect respiration. current research on insect DGCs is driven by three adaptive hypotheses explaining the origin or maintenance of DGCs among insects. They propose that discontinuous gas ex- Introduction change evolved or is currently maintained in order to (1) Insects maintain the highest mass-specific rates of oxygen reduce respiratory water-loss (hygric hypothesis; Buck and consumption found in the animal kingdom by eschewing Keister 1955), (2) enhance gas exchange in subterranean the complex pulmonary and circulatory systems used by atmospheres (chthonic hypothesis; Lighton 1998), and (3) most other animals (Suarez 2000). Instead, they use an ameliorate the toxic effects of near-ambient intratracheal extensive network of air-filled tubes, called tracheae, which oxygen levels (oxidative damage hypothesis; Bradley 2000). branch and ramify throughout all parts of their body, pro- However, the wide range of environments occupied by viding an air-filled pathway for the rapid movement of insects that display DGCs (from mesic to hyperarid, sub- oxygen and carbon dioxide directly between the insect’s terranean to terrestrial), as well as their diverse life strategies tissues and the surrounding atmosphere. Since the insect’s (flying and flightless, adult and pupal), makes identifying a cuticle is largely impermeable to gas diffusion, this “tra- common adaptive benefit difficult. As each of these hy- cheal system” opens to the environment through spiracles, potheses predicts a different relationship between DGC du- small pores located along the lateral margins of the insect’s ration and ambient temperature, humidity, oxygen partial body. Spiracles contain muscular valves that permit or pressure, or some combination of these variables, a recent restrict gas exchange by opening and closing, thus enabling study by White et al. (2007) used a strong inference ap- insects to display a range of respiratory gas exchange pat- proach to determine which of these hypotheses is best sup- terns from continuous to periodic. The discontinuous gas ported by the current data. While this study found support for the hygric hypothesis and some support for the oxidative * Corresponding author; e-mail: [email protected]. damage hypothesis on the basis of longer DGC cycles among Am. Nat. 2011. Vol. 177, pp. 130–134. ᭧ 2010 by The University of Chicago. insects from higher temperature and lower rainfall envi- 0003-0147/2011/17701-52218$15.00. All rights reserved. ronments, this conclusion assumes explicitly that of the DOI: 10.1086/657619 three hypotheses tested, one must be correct. This is not This content downloaded from 23.235.32.0 on Tue, 6 Oct 2015 21:47:02 PM All use subject to JSTOR Terms and Conditions Discontinuous Gas Exchange in Insects 131 necessarily the case (O’Donohue and Buchanan 2001). from the brain (Miller 1960; Myers and Retzlaff 1963). In Given that DGCs appear to have evolved independently five various grasshoppers and cockroaches the thoracic and times (Marais et al. 2005), there are potentially between one abdominal ganglia have been shown to possess both spon- and five explanations for their origin and perhaps many taneous rhythm generators (Bustami and Hustert 2000) more adaptive hypotheses explaining their current function and chemosensitivity to O2 and CO2 (Case 1957; Miller or functions. This would certainly account for the equivocal 1960; Edwards and Miller 1986; Bustami et al. 2002). It support that these hypotheses receive. As has been pointed is then the interplay between their CO2 and O2 “set points” out, insect DGCs could result from multiple causal mech- and how they each stimulate spiracular opening, that re- anisms among the various insect groups, making a universal sults in the emergence of DGCs (Fo¨rster and Hetz 2009). adaptive explanation for their occurrence unrealistic The importance of brain activity in controlling the (Chown 2002). Thus, before we continue to conceive and emergence of DGCs can also be seen among the different test adaptive hypotheses, there is a fundamental question castes in ant colonies. All queen ants investigated so far that must first be addressed: What is the underlying mech- have been shown to display pronounced DGCs, while anistic basis driving DGCs and is this mechanism the same members of their worker caste generally do not (Lighton among all insects? et al. 1993a; Lighton and Berrigan 1995). This difference More than 50 years of research into insect respiratory was considered to be evidence of adaptation by the queens control provides a wealth of evidence that strongly suggests to the potential respiratory challenges of their subterra- there is one thing that all insects displaying DGCs have nean environment (Lighton 1998). However, morpholog- in common: reduced or absent brain activity. Experiments ical studies have found that while virgin queen ants have have demonstrated that decapitated cockroaches sponta- larger brains than the worker caste (Ehmer and Gronen- neously display DGCs (Edwards and Miller 1986), as do berg 2004), their brains undergo a significant reduction both decapitated and anesthetized ants (Lighton et al. in size immediately following mating and the onset of the 1993b; Lighton and Garrigan 1995; Duncan and Newton underground, egg-laying phase of their life cycle (Julian 2000) and diapausing pupa with or without their brains and Gronenberg 2002). Thus, queen ants may display removed (Levy and Schneiderman 1966). Evidently, in- DGCs not because of any subterranean respiratory stress capacitating or removing the brain reveals a periodic pat- but because of a reduction in brain size and activity as- tern of ventilation. That headless insects can continue to sociated with the reduced behavioral repertoires and a lack ventilate at all is due to the decentralized nature of their of visual stimulation
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