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Tracheal Respiration in Insects Visualized with Synchrotron X-ray Imaging

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Science  24 Jan 2003:
Vol. 299, Issue 5606, pp. 558-560
DOI: 10.1126/science.1078008

Abstract

Insects are known to exchange respiratory gases in their system of tracheal tubes by using either diffusion or changes in internal pressure that are produced through body motion or hemolymph circulation. However, the inability to see inside living insects has limited our understanding of their respiration mechanisms. We used a synchrotron beam to obtain x-ray videos of living, breathing insects. Beetles, crickets, and ants exhibited rapid cycles of tracheal compression and expansion in the head and thorax. Body movements and hemolymph circulation cannot account for these cycles; therefore, our observations demonstrate a previously unknown mechanism of respiration in insects analogous to the inflation and deflation of vertebrate lungs.

Respiratory mechanisms in insects are important to our understanding of the physiology, behavior, and evolution of this diverse animal group. Most insects respire through a system of tubes called tracheae that connect to the air via spiracles that can be actively opened or closed (1). Tracheal tubes form a complex network of gas-filled vessels that divide throughout the body segments, legs, and wings. The tiniest tubes, called tracheoles, may be 1 μm in diameter, and they function to exchange gas with tissues of the body. Mechanisms for insect respiration include passive gas diffusion (2,3), changes in internal pressure due to hemolymph pumping by the heart or by muscle contraction in the abdomen (4,5), and autoventilation, during which body movements change the volume of tracheal tubes or air sacs associated with the tracheae (6–8). Despite recent insights into these active mechanisms for changing the volume of the tracheal system (8, 9), the internal mechanics of insect respiration are largely unknown.

To directly observe changes in volume of the insect tracheal system, we obtained high-resolution x-ray videos of living insects using 15- to 25-keV synchrotron x-rays [supporting online material (SOM) Text]. The high flux and partial coherence of the x-ray source allow for real-time, phase-enhanced imaging (10) in which edge enhancement of the images enables clear visualization of insect anatomy. X-ray videos were recorded for the anterior thorax and head regions of ground beetles (Platynus decentis), carpenter ants (Camponotus pennsylvanicus), house crickets (Achaeta domesticus), and other insects in either dorsal or lateral view.

The tracheal system at rest was inflated and was clearly visible as bright branching patterns on the x-ray video (Fig. 1; Movie S1). During compression, tracheae were squeezed to a progressively smaller diameter tube over the course of 300 to 500 ms and then were expanded over a similar time course. No changes in length of tracheae were observed. Tracheae were compressed in one primary direction (either laterally or dorsoventrally) so that the roughly circular cross section of the trachea at rest was compressed into an ellipse. For example, in beetles, lateral compression of the main thoracic tracheae was indicated by a decrease in tracheal width when viewed dorsally, and this appeared as a slight increase in width from a lateral view (Fig. 1). Narrowing of the tracheae was often synchronous throughout the head and thorax, but local tracheal compression was also observed.

Figure 1

Respiration by tracheal compression in the head and thorax of the beetle Platynus decentis (see Movie S1). Left panels are dorsoventral view (head, up; sides, left and right), right panels are lateral view (head, up; ventral, left) of different beetles. Tracheal tubes are expanded at rest [(A), arrowhead e], and compression (B) occurs throughout the anterior region of the insect. Lateral compression results in narrower tracheae in dorsal view and wider tracheae in lateral view. Maximal compression [(C), arrowhead c] is followed quickly by expansion of the tracheae (D). The entire respiratory cycle is completed in less than 1 s.

Respiratory frequency (Fig. 2) ranged from about 0.4 Hz to 0.7 Hz in the beetle (SOM Text). Duration of compression ranged from about 0.7 to 1.6 s in the three species (Fig. 2), followed by a period of inactivity. These data indicate interspecific variability in both exhalation-inhalation duration and cycle frequency. Volume change of tracheal tubes during respiration was calculated with the use of data on length and width of the tracheae during respiratory cycles (SOM Text). Volume change in the major tracheae of the anterior thorax and basal head of all three species was nearly 50% (Fig. 3). Mean resting volume of the main tracheal trunks of beetles was 0.065 mm3, and at maximal compression there was a volume decrease of 0.03 mm3, representing a tidal volume of 46%. Ants had the same average respiratory capacity (tidal volume of 46%), whereas crickets expelled less gas, with a tidal volume of 36%. All three species also showed deflation of the small subdivisions of the tracheae, suggesting that similar volume changes may be achieved throughout the tracheal system.

Figure 2

Cycle frequency and compression duration of respiration in three insect species: the wood beetle, house cricket, and carpenter ant. Frequency of respiratory cycles was variable, ranging from 0.4 to 0.7 Hz, and the total time of tracheal compression ranged from about 0.7 to 1.6 s among species. Error bars, 1 standard deviation.

Figure 3

Volume change in the main tracheae of the anterior thorax and head of the wood beetle, house cricket, and carpenter ant during respiratory cycles. Error bars, standard deviation of the mean of three respiratory pumping events in different individuals.

The rapid tracheal compression in insects signifies a previously undescribed active mechanism of respiration. We observed other respiratory mechanisms, such as abdominal pumping (4,9), autoventilation (6), and circulatory fluid motion. However, these mechanisms cannot account for the rapid changes in head and thorax volume shown by synchrotron imaging. Tracheal compression in insects functions as a mechanism of air convection much like that of vertebrate lungs. The resting lung ventilation of a human, for example, is about 10% but may reach 75% during exercise; similar values have been measured for birds (6, 12). The insects studied here with 50% tidal volume were likely respiring at high rates, perhaps similar to the rates used during exercise, stress, or flight (3,13). A second function of tracheal compression is to aid oxygen diffusion to tissues. If tracheal compression occurs with the spiracles closed, increased pressure will raise the diffusion gradient of oxygen across the tracheole-tissue boundary.

The mechanism of tracheal compression is likely driven by contraction of jaw muscles or limb muscles, causing elevated pressure inside the exoskeleton (14–17). Upon relaxation of the muscle, the tracheae expand due to the support from rings of taenidia in the tracheal wall (1) in a manner similar to recoil aspiration in air-breathing fishes (18). This mechanism implies the linking of locomotor muscles to respiration, which has been found to be widespread among animals (19).

Active tracheal breathing in the head and thorax may have played an important role in the evolution of terrestrial locomotion, running performance, and flight in insects, and it may be a prerequisite for oxygen delivery to complex sensory systems and active feeding mechanisms. Tracheal compression appears widespread but not ubiquitous among insect lineages. We observed this mechanism of active tracheal respiration in some members of diverse groups of endopterygote insects (beetles, butterflies, flies) as well as in Hemiptera (bugs), the Orthoptera (cricket), Dermaptera (earwigs), Blattodea (cockroaches), and more basal insect lineages such as Odonata (dragonflies). The spectacular diversity of insects likely includes a range of respiratory mechanisms, some of which depend on the compression and expansion of the tracheal system in a lung-like manner as the means to exchange gases with the environment.

Supporting Online Material

www.sciencemag.org/cgi/content/full/299/5606/558/DC1

Materials and Methods

Movie S1

  • * To whom correspondence should be addressed. E-mail: mwestneat{at}fieldmuseum.org

REFERENCES AND NOTES

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