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First published online October 17, 2008
Journal of Experimental Biology 211, 3409-3420 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.019877
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Correlated patterns of tracheal compression and convective gas exchange in a carabid beetle

John J. Socha1,*, Wah-Keat Lee1, Jon F. Harrison2, James S. Waters3, Kamel Fezzaa1 and Mark W. Westneat3

1 Advanced Photon Source, Argonne National Laboratory, Argonne, IL 60439, USA
2 Section of Organismal, Integrative and Systems Biology, Arizona State University, Tempe, AZ 85287, USA
3 Department of Zoology, Field Museum of Natural History, Chicago, IL 60605, USA


Figure 1
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  		Fig. 1. Experimental setup used to simultaneously record CO2 emission and visualize internal tracheal compression of the carabid beetle Pterostichus stygicus. Multiple locations in the body were recorded; x-ray movie stills here show tracheal tubes in the mesothorax between first and second coxae (large circular cuticular joints). The blue arrow indicates the location where we digitized the primary tube depicted in Fig. 3. Field of view is 3.2 mmx2.4 mm. In the schematic diagram, legs are not depicted for clarity, but were tucked to the side of the beetle.

 

Figure 2
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  		Fig. 2. Occurrence of rhythmic tracheal compression in different regions of the body of Pterostichus stygicus. (A) Tracheal system, showing tracheae in resting (inflated) posture. Image is a compilation of multiple x-ray images of a freshly killed specimen. Posterior abdomen not shown. (B–E) Movie stills showing inflated (left image) and compressed (right image) tracheae, depicting compression in the prothorax (B), mesothorax (C), metathorax (D) and posterior abdomen (E). Asterisks mark tracheal tubes that are compressed in the corresponding image. Compressions also occurred in the head and legs (not shown). Scale bars: 1 mm (A), 200 µm (B–E).

 

Figure 3
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  		Fig. 3. Kinematics of tracheal compression in Pterostichus stygicus. Data depict width changes at one location (Fig. 1, blue arrow) of a primary tracheal tube located in the mesothorax. For comparison, the compression cycles are overlaid at time zero. (A,B) Variation in compression cycles within two individual beetles. In A, the beetle (mass 193.0 mg) used similar compression and reinflation dynamics, but with variable duration of the compressed phase. The beetle in B (mass 155.7 mg) displayed highly regular compression cycles. (C) Average compression cycles for five individuals. Each line represents an average of five compression cycles for each individual. (D) Summary of compression dynamics: i, collapse; ii, static compression; iii, reinflation. Blue line represents the average of the five individuals in C, each normalized to percentage width and percentage time. Gray shading represents 1 s.d. from the mean.

 

Figure 4
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  		Fig. 4. Correlation of tracheal compressions with respiratory pulses of CO2 in Pterostichus stygicus. Data are from one trial (mass 280.0 mg) showing representative CO2 emission before x-ray exposure (A), during x-ray exposure (B), and after x-ray exposure (C). Green vertical lines indicate the start of a tracheal compression, identified from x-ray movie records (digitized block between pair of arrows, t=3.8 min). The inset box in C depicts a simulated CO2 trace using a 1/10 slower flow speed: 150 ml min–1 (purple) vs 1.5 l min–1 (gray). To simulate the slower speed, CO2 data were smoothed using a running average of 15 points (4.5 s); this interval was chosen to approximate the transit time of gas through the infrared detector at this flow speed (see Gray and Bradley, 2006Go). Simulated low flow speeds obscure the prominent high-frequency component of the signal.

 

Figure 5
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  		Fig. 5. Details of the relative timing of tracheal compressions and CO2 pulses in different regions of the body of Pterostichus stygicus. Gray banding represents the total duration of the compression cycle (from collapse to reinflation), identified from movie records. The green lines indicate the start of compression, with line thickness representing the duration of tracheal collapse phase. The boxes above each trace indicate which part of the beetle was in (x-ray) view during CO2 recording; arrows represent translation of the beetle to a different body region. Data are from one specimen (mass 130.0 mg).

 

Figure 6
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  		Fig. 6. (A) Occurrence of CO2 pulses from zero and non-zero baseline CO2 in one specimen of Pterostichus stygicus. `Singlet' pulses (indicated with grey arrows) were stand-alone bursts of CO2 that occurred with a tracheal compression. Such singlets did not occur in any other specimen. The inset box shows the area (red) used to calculate the volume of all other pulses. Beetle, mass 178.0 mg. (B) Multiple repeating CO2 bursts used to simulate patterns of superimposition (without additional CO2). A large singlet burst (red arrow in A) was repeated at frequencies (f) of 14, 20, 33 and 50 min–1.

 

Figure 7
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  		Fig. 7. Effect of x-ray beam on CO2 release in Pterostichus stygicus. Traces from two specimens are shown, depicting extremes of the response to irradiation. The beetle (mass 219.5 mg) in A shows no change in average CO2 pulse frequency (15.7 min–1) or volume (0.013 µl), whereas the beetle (mass 166.3 mg) in B shows an increase in both frequency (8.1 to 16.2 min–1) and volume (0.004 to 0.024 µl).

 

Figure 8
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  		Fig. 8. Comparison of gas exchange patterns during pre-beam, beam on and post-beam treatments. Only CO2 pulse volume (C) showed significant differences (asterisk); beam on volumes were greater than those of both pre- and post-beam. The top, bottom and line through the middle of the box correspond to the 75th, 25th and 50th percentile (median), respectively; whiskers extend from the 10th and 90th percentiles.

 

Figure 9
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  		Fig. 9. Model of the tracheal system used to estimate the volume of displaced air during a tracheal compression in Pterostichus stygicus. Black ovals depict the thoracic spiracles. The main trachea of each femur was used (six total); only one is depicted for clarity.

 

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© The Company of Biologists Ltd 2008