Regulation of Respiration in Lower Vertebrates: Role of CO2/pH Chemoreceptors

SUMMARYThe aim of the present study was to determine the roles that externally versus internally oriented CO 2 /H + -sensitive chemoreceptors might play in promoting cardiorespiratory responses to environmental hypercarbia in the air-breathing fish, Hoplerythrinus unitaeniatus (jeju). Fish were exposed to graded hypercarbia (1, 2.5, 5, 10 and 20% CO 2 ) and also to graded levels of environmental acidosis (pH ~7.0, 6.0, 5.8, 5.6, 5.3 and 4.7) equal to the pH levels of the hypercarbic water to distinguish the relative roles of CO 2 versus H + . We also injected boluses of CO 2 -equilibrated solutions (5, 10 and 20% CO 2 ) and acid solutions equilibrated to the same pH as the CO 2 boluses into the caudal vein (internal) and buccal cavity (external) to distinguish between internal and external stimuli. The putative location of the chemoreceptors was determined by bilateral denervation of branches of cranial nerves IX (glossopharyngeal) and X (vagus) to the gills. The data indicate that the chemoreceptors eliciting bradycardia, hypertension and gill ventilatory responses (increased frequency and amplitude) to hypercarbia are exclusively branchial, externally oriented and respond specifically to changes in CO 2 and not H + . Those involved in producing the cardiovascular responses appeared to be distributed across all gill arches while those involved in the gill ventilatory responses were located primarily on the first gill arch. Higher levels of aquatic CO 2 depressed gill ventilation and stimulated air breathing. The chemoreceptors involved in producing air breathing in response to hypercarbia also appeared to be branchial, distributed across all gill arches and responded specifically to changes in aquatic CO 2 . This would suggest that chemoreceptor groups with different orientations (blood versus water) are involved in eliciting air-breathing responses to hypercarbia in jeju.Key words: gills, cardiorespiratory control, hypercarbia, CO 2 and H + chemoreceptors, air breathing, jeju, Hoplerythrinus unitaeniatus. THE JOURNAL OF EXPERIMENTAL BIOLOGY 2798and Baird, 1982; Graham, 1997;Sanchez et al., 2005). In other species, however, increases in environmental CO 2 are without effect on gill ventilation (Johansen, 1966;Todd, 1972;McMahon and Burggren, 1987) or air breathing (Johansen et al., 1968;Lomholt and Johansen, 1974). Just as with aquatic CO 2 , some air-breathing fish show no response to increasing levels of CO 2 in inspired air Perry et al., 2008) while others show an increase (Smith, 1930; Delaney et al., 1974; Delaney et al., 1976; Delaney et al., 1977; Babiker, 1979) or even a decrease (Jesse et al., 1967) in ventilation of the air-breathing organ (ABO).The equivocal nature of the data raises questions about the existence and role of internally oriented CO 2 /H + -sensitive chemoreceptors in driving gill ventilation in exclusively waterbreathing fish, as well as in driving gill ventilation or air breathing in facultative and obligate air-breathing fish. Clearly much remains to be done to resolve this issue...

“…Similar results have been obtained in several other studies (reviewed by Milsom, 1995a;Milsom, 1995b;Milsom, 2002;Gilmour, 2001;Perry and Gilmour, 2002;Gilmour and Perry, 2007).…”

Section: The Co 2 Threshold For Eliciting Cardiorespiratory Responsessupporting

confidence: 91%

Section: Introductionmentioning

confidence: 99%

Hypercarbic cardiorespiratory reflexes in the facultative air-breathing fish jeju (Hoplerythrinus unitaeniatus): the role of branchial CO2 chemoreceptors

Boijink

Florindo

Leite

et al. 2010

“…The blunting of the breathing pattern response to gestation during hypercapnia may indicate a decreased sensitivity of CO 2 chemoreceptors during pregnancy. The sensitivity of pulmonary stretch receptors (which are mildly CO 2 sensitive) is depressed by hypercapnia, which reduces the negative feedback during lung inflation, and results in elevated V T (Milsom, 1995;Powell et al, 1988). In addition, hypercapnic stimulation of pulmonary and upper airway chemoreceptors has been shown to reduce f (and hence V E ) in tegus (Ballam, 1985;Ballam and Donaldson, 1988;Coates et al, 1991).…”

Section: Breathing Patterns In Response To Hypercapniamentioning

confidence: 99%

“…Estimates of the cost of breathing in reptiles range from 1 to 52%: 1-15% in hatchling alligators (Wang and Warburton, 1995), up to 17% for fasted and digesting tegu lizards (Skovgaard and Wang, 2004), 52% in dormant tegus (de Andrade and Abe, 1999) and 1-30% in chelonians (Jackson et al, 1991;Kinney and White, 1977). In contrast, most mammals have relatively low energetic costs of breathing, averaging between 1 and 7% (Milsom, 1989;Milsom, 1995). However, the energetic cost of breathing may increase significantly in some circumstances, for example, disease states such as chronic obstructive pulmonary disease (emphysema, chronic bronchitis or a mixture of both) in humans (Dellweg et al, 2008;Jounieaux and Mayeux, 1995).…”

Section: Introductionmentioning

confidence: 99%

Gestation increases the energetic cost of breathing in the lizard, Tiliqua rugosa

Munns

2012

SUMMARYHigh gestational loads result in fetuses that occupy a large proportion of the body cavity and may compress maternal organs. Compression of the lungs results in alterations in breathing patterns during gestation, which may affect the energetic cost of breathing. In this study, the energetic cost of breathing during gestation was determined in the viviparous skink Tiliqua rugosa. Radiographic imaging showed progressive lung compression during gestation and a 30% reduction in the lung inflation index (rib number at which the caudal margin of the lung was imaged divided by total rib number). Pneumotachography and open flow respirometry were used to measure breathing patterns and metabolic rates. Gestation induced a twofold increase in minute ventilation via increases in breathing frequency, but no change in inspired tidal volume. The rates of O 2 consumption and CO 2 production did not change significantly during gestation. Together, these results suggest that a relative hyperventilation occurs during gestation in T. rugosa, which in turn suggests that diffusion and/or perfusion limitations may exist at the lung during gestation. The energetic cost of breathing was estimated as a percentage of resting metabolic rate using hypercapnia to stimulate ventilation at different stages of pregnancy. The energetic cost of breathing in non-pregnant lizards was 19.96±3.85% of resting metabolic rate and increased threefold to 62.80±10.11% during late gestation. This significant increase in the energetic cost of breathing may have significant consequences for energy budgets during gestation.

“…The implication of this finding is that P. annectens, like tetrapod vertebrates, possesses CO 2 and/or pH-sensitive chemoreceptors that monitor the status of the body fluids. In tetrapods, central and peripheral CO 2 /pHsensitive chemoreceptors initiate ventilatory adjustments for acid-base regulation (reviewed by Gonzalez et al, 1994;Milsom, 1995;Milsom, 2002;Taylor et al, 1999). By contrast, the balance of evidence suggests that strictly water-breathing fish lack internally oriented CO 2 /pH chemoreceptors -central chemoreceptors appear to be absent, and ventilatory chemoreflexes are dominated by branchial chemoreceptors that respond primarily to changes in water CO 2 (reviewed by Gilmour and Perry, 2007).…”

Section: Discussionmentioning

confidence: 99%

Mechanisms of acid–base regulation in the African lungfishProtopterus annectens

Gilmour

Euverman

Esbaugh

et al. 2007

cotransporter) were cloned, and their branchial and renal mRNA expressions were examined prior to and following acid or base infusion. In no case was mRNA expression significantly altered by metabolic acid-base disturbance. These findings suggest that lungfish, like tetrapods, alter ventilation to compensate for metabolic acid-base disturbances, a mechanism that is not employed by waterbreathing fish. Like fish and amphibians, however, extrarenal routes play a key role in metabolic compensation.