Cardiovascular and respiratory reflexes in the tropical fish, traira (Hoplias malabaricus): CO2/pH chemoresponses

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...

supporting

confidence: 92%

“…traíra (Gilmour and Perry, 1996;Reid et al, 2000;Sundin et al, 2000;. They also had no effect in jeju in the present study.…”

supporting

confidence: 45%

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

Boijink

Florindo

Leite

et al. 2010

“…Typically, most species that have been examined exhibit hyperventilation that is mediated by increases in breathing frequency and/or ventilatory stroke volume (Dejours, 1973;Janssen and Randall, 1975;Randall et al, 1976;Smatresk and Cameron, 1982;Perry and Gilmour, 1996;Crocker et al, 2000;Perry et al, 2009b) (for reviews, see Shelton et al, 1986;Perry and Wood, 1989;Milsom, 1995;Gilmour, 2001;Perry and Gilmour, 2002;Gilmour and Perry, 2007;Perry et al, 2009a;Perry and Abdallah, 2012). The cardiovascular responses to hypercapnia have received less attention but in those few species that have been examined, a conserved response appears to be bradycardia Sundin et al, 2000;Reid et al, 2000;Perry and McKendry, 2001;Gilmour et al, 2005) which may, or may not, be associated with an increase in arterial blood pressure (reviewed by Gilmour and Perry, 2007). Bradycardia, however, is not a universal response to hypercapnia; two species were shown to exhibit tachycardia [Acipenser transmontanus (Crocker et al, 2000) and Tinca tinca (Randall and Shelton, 1963)] and in others, cardiac frequency is unaltered (Gilmour and Perry, 2007).…”

Section: Introductionmentioning

confidence: 99%

Cardiac responses to hypercapnia in larval zebrafish (Danio rerio): The links between CO2 chemoreception, catecholamines and carbonic anhydrase

Miller

Pollack

Bradshaw

et al. 2014

The ontogeny of carbon dioxide (CO 2 ) sensing in zebrafish (Danio rerio) has not been examined. In this study, CO 2 -mediated increases in heart rate were used to gauge the capacity of zebrafish larvae to sense CO 2 . CO 2 is thought to be detected via neuroepithelial cells (NECs), which are homologous to mammalian carotid body glomus cells. Larvae at 5 days post-fertilization (d.p.f.) exhibited tachycardia when exposed for 30 min to 0.75% CO 2 (~5.63 mmHg); at 7 d.p.f., tachycardia was elicited by 0.5% CO 2 (~3.75 mmHg). Based on pharmacological evidence using β-adrenergic receptor (β-AR) antagonists, and confirmed by β 1 -AR translational gene knockdown using morpholinos, the reflex tachycardia accompanying hypercapnia was probably mediated by the interaction of catecholamines with cardiac β 1 receptors. Because the cardiac response to hypercapnia was abolished by the ganglionic blocker hexamethonium, it is probable that the reflex cardio-acceleration was mediated by catecholamines derived from sympathetic adrenergic neurons. Owing to its likely role in facilitating intracellular acidification during exposure to hypercapnia, it was hypothesized that carbonic anhydrase (CA) is involved in CO 2 sensing, and that inhibition of CA activity would blunt the downstream responses. Indeed, the cardiac response to hypercapnia (0.75% CO 2 ) was reduced in fish at 5 d.p.f. exposed to acetazolamide, a CA inhibitor, and in fish experiencing zCAc (CA2-like a) knockdown. Successful knockdown of zCAc was confirmed by CA activity measurements, western blotting and immunocytochemistry. Co-injection of embryos with zCAc morpholino and mRNA modified at the morpholino binding site restored normal levels of CA activity and protein levels, and restored (rescued) the usual cardiac responses to hypercapnia. These data, combined with the finding that zCAc is expressed in NECs located on the skin, suggest that the afferent limb of the CO 2 -induced cardiac reflex in zebrafish larvae is initiated by coetaneous CO 2 -sensing neuroepithelial cells.

“…The tambaqui is a hypoxia-tolerant (P 50 =2.4·mmHg; Brauner et al, 2001) and hypercarbia-tolerant neotropical fish species that is found throughout the Amazon basin, often in floodplain lakes that are subject to large variations in O 2 , CO 2 and pH. Owing to the frequent occurrence of hypercarbic conditions in its natural environment (water total dissolved CO 2 may range from 0.82 to 1.79·mmol·l -1 depending on season and depth; Reid et al, 2000), and an anatomy that renders this species amenable to surgical sectioning of nerves innervating selected chemosensory areas, the tambaqui has been the focus of a concerted research effort to identify the locations and roles of chemoreceptors involved in respiratory reflexes to both hypoxia and hypercarbia Milsom et al, 2002;Reid et al, 2003;Florindo et al, 2004). Previous studies have focused primarily on reflex changes in ventilation and heart rate during hypoxic or hypercarbic exposures without monitoring blood gas or acid-base status.…”

mentioning

confidence: 99%

Cardiorespiratory responses to hypercarbia in tambaquiColossoma macropomum: chemoreceptor orientation and specificity

Gilmour

Milsom

Rantin

et al. 2005

SUMMARY Experiments were carried out to test the hypothesis that ventilatory and cardiovascular responses to hypercarbia (elevated water PCO2) in the tambaqui Colossoma macropomum are stimulated by externally oriented receptors that are sensitive to water CO2 tension as opposed to water pH. Cardiorespiratory responses to acute hypercarbia were evaluated in both the absence and presence of internal hypercarbia (elevated blood PCO2), achieved by treating fish with the carbonic anhydrase inhibitor acetazolamide. Exposure to acute hypercarbia (15 min at each level, final water CO2 tensions of 7.2,15.5 and 26.3 mmHg) elicited significant increases in ventilation frequency(at 26.3 mmHg, a 42% increase over the normocarbic value) and amplitude(128%), together with a fall in heart rate (35%) and an increase in cardiac stroke volume (62%). Rapid washout of CO2 from the water reversed these effects, and the timing of the changes in cardiorespiratory variables corresponded more closely to the fall in water PCO2(PwCO2) than to that in blood PCO2(PaCO2). Similar responses to acute hypercarbia (15 min,final PwCO2 of 13.6 mmHg) were observed in acetazolamide-treated (30 mg kg-1) tambaqui. Acetazolamide treatment itself, however, increased PaCO2 (from 4.81±0.58 to 13.83±0.91 mmHg, mean ± s.e.m.; N=8) in the absence of significant change in ventilation, heart rate or cardiac stroke volume. The lack of response to changes in blood PCO2 and/or pH were confirmed by comparing responses to the bolus injection of hypercarbic saline(5% or 10% CO2; 2 ml kg-1) into the caudal vein with those to the injection of CO2-enriched water (1%, 3%, 5% or 10%CO2; 50 ml kg-1) into the buccal cavity. Whereas injections of hypercarbic saline were ineffective in eliciting cardiorespiratory responses, changes in ventilation and cardiovascular parameters accompanied injection of CO2-laden water into the mouth. Similar injections of CO2-free water acidified to the corresponding pH of the hypercarbic water (pH 6.3, 5.6, 5.3 or 4.9, respectively) generally did not stimulate cardiorespiratory responses. These results are in agreement with the hypothesis that in tambaqui, externally oriented chemoreceptors that are predominantly activated by increases in water PCO2,rather than by accompanying decreases in water pH, are linked to the initiation of cardiorespiratory responses to hypercarbia.