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Air-breathing in the bowfin (Amia calva L.)

University of British Columbia

The control of air-breathing in the bowfin, Amia calva, was investigated using experimental and analytical approaches. The air-breathing pattern of conscious, undisturbed bowfin at 22±2 °C was characterized by the responses to changes in respiratory gases in the aquatic and aerial environments. Pneumotachographic measurements of air flows during air-breathing events revealed two distinct patterns: in type I breaths exhalation was followed by inhalation; in type II air breaths, which have not been described for this species, only inhalation occurred. Under normoxic conditions both types of air breaths occurred (60% type I:40% type II) and the mean inter-breath interval was 19.8±0.9 (95% C.I.) min. Aquatic or aerial hypoxia stimulated air-breathing, IBI decreased to about 13 min in both conditions, and there was a change in air-breathing pattern to predominantly type I air breaths (>80% of total breaths). Maximum expired volume for type I breaths averaged 25.1±6.2 ml kg⁻¹. Air bladder volume was 80 ml kg⁻¹, so that about 30% of total air bladder volume was exchanged during a type I breath. Bowfin exposed to 100% O₂ in the aerial phase, regardless of aquatic PO₂, switched to type II air breaths almost exclusively (>99% of total breaths). Air bladder deflation in conscious fish initially resulted in only type II air breaths being taken. The time to initiate an air breath and the number of air breaths following deflation were both significantly dependent upon the volume removed from the air bladder. The results suggest that dynamic and static characteristics of air bladder mechanoreceptors are involved in the afferent limb of the type II breathing response and that type II breaths serve a buoyancy, rather than gas exchange, function. Branchial denervation was used to test the hypothesis that type I air breaths were stimulated by O₂-chemoreceptors located on the gills. Bowfin were either sham-operated (SH), partially-denervated (PD) or totally-denervated (TD) and exposed to aquatic normoxia and aquatic hypoxia. Air-breathing frequency, measured as total breaths, increased from aguatic normoxia to hypoxia in all three groups; air-breathing frequency was significantly higher in the TD group. This was due, however, to large numbers of type II air breaths occurring between 0 and 1 min as a result of excessive loss of inspired gas during inhalation. There was no significant difference in the frequency of type I breaths for any group when analyzed separately from type II breaths; thus, the afferent limb of the air-breathing response to hypoxia was not identified, suggesting that extra-branchial sites for O₂-chemorception may be involved. The results also indicate that either sensory or motor components of nerves IX and X to the gill arches are important for proper air-breathing function. The role of central chemosensitivity was examined by perfusing a mock extra-dural fluid equilibrated with normoxic, hyperoxic, hypoxic or hypercapnic gas mixtures through the cranial space in conscious fish. Air-breathing was only stimulated by aquatic hypoxia, not changes in extra-dural fluid composition, thus implicating peripheral.sites for O₂-mediated effects on aerial ventilation. Unfortunately, these results, along with gill denervation data, do not yield any information about the location of O₂-chemosensitive sites or afferent pathways that modulate air-breathing in bowfin. The temporal, intermittent pattern of air-breathing was examined by spectral analysis. The intermittent pattern was found to have significant, non-random frequency components. A significant low frequency component, corresponding with a 30 min period, was found in the periodogram of 6 bowfin in nor-moxic conditions. In aquatic or aerial hypoxia, the dominant periods ranged between 5 and 10 min. The dominant periodicities in normoxia, or either hypoxic condition, were correlated with the mean inter-breath interval for type I breaths. Since type I breaths were affected by changes in external and/or internal PO₂, the results indicate that air-breathing behavior occurs periodically and may be driven by O₂-sensitive chemore-ceptors. A computer model was formulated to simulate the intermittent air-breathing pattern. The model used two independent thresholds for triggering type I and type II air breaths. Type I air breaths were modeled as threshold responses to reductions in intravascular PO₂. Type II air breaths were simulated as feedback responses to reductions in air bladder volume. Using empirical data from this study and other published work, the model produced intermittent air-breathing simulations that closely resembled the responses of bowfin exposed to aerial normoxia, hypoxia and hyperoxia. Quantitative and qualitative similarities between the model and data from bowfin suggest the model is realistic in its assumptions regarding mechano- and chemoreceptive inputs controlling intermittent air-breathing. The results from this study indicate that bowfin normally use two types of respiratory behaviors that serve gas exchange and buoyancy functions. Intermittent breathing in this species is shown to be periodic, and the rhythmicity appears to be generated by feedback from O₂-sensitive chemoreceptors located in a position to monitor intra-vascular changes in PO₂.

Text

2011-01-31

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http://hdl.handle.net/2429/31020

Zoology

University of British Columbia

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