Hypoxic cardiorespiratory reflexes in the facultative air-breathing fish jeju (Hoplerythrinus unitaeniatus): Role of branchial O2 chemoreceptors

Department of Physiological Sciences, Federal University of São Carlos, Via Washington Luiz, km 235, São Carlos, SP, 13565-905, Brazil.
Journal of Comparative Physiology B (Impact Factor: 2.62). 03/2010; 180(6):797-811. DOI: 10.1007/s00360-010-0461-2
Source: PubMed


In one series of experiments, heart frequency (f (H)), blood pressure (P (a)), gill ventilation frequency (f ( R )), ventilation amplitude (V (AMP)) and total gill ventilation (V (TOT)) were measured in intact jeju (Hoplerythrinus unitaeniatus) and jeju with progressive denervation of the branchial branches of cranial nerves IX (glossopharyngeal) and X (vagus) without access to air. When these fish were submitted to graded hypoxia (water PO(2) approximately 140, normoxia to 17 mmHg, severe hypoxia), they increased f ( R ), V (AMP), V (TOT) and P (a) and decreased f (H). In a second series of experiments, air-breathing frequency (f (RA)), measured in fish with access to the surface, increased with graded hypoxia. In both series, bilateral denervation of all gill arches eliminated the responses to graded hypoxia. Based on the effects of internal (caudal vein, 150 microg NaCN in 0.2 mL saline) and external (buccal) injections of NaCN (500 microg NaCN in 1.0 mL water) on f (R), V (AMP), V (TOT), P (a) and f (H) we conclude that the O(2) receptors involved in eliciting changes in gill ventilation and associated cardiovascular responses are present on all gill arches and monitor the O(2) levels of both inspired water and blood perfusing the gills. We also conclude that air breathing arises solely from stimulation of branchial chemoreceptors and support the hypothesis that internal hypoxaemia is the primary drive to air breathing.

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    • "In studies conducted with Hoplias malabaricus (Sundin et al., 1999), Hoplias lacerdae (Micheli-Campbell et al., 2009), Hoplerythrinus unitaeniatus (Lopes et al., 2010), Colossoma macropomum (Sundin et al., 2000) and Piaractus mesopotamicus (Leite et al., 2007), fish had their local reflexes abolished by sectioning specific cranial nerves innervating gill arches. In those studies, the cranial nerves (IX to the first pair of gill arches and X for the first and other gill arches) could be accessed by a small incision in the epithelium at the dorsal end of the gill arches where they meet the roof of the opercular cavity. "
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    ABSTRACT: We evaluated the role of the first pair of gill arches in control of cardiorespiratory responses to normoxia and hypoxia in the air-breathing catfish, Clarias gariepinus. An intact group (IG) and an experimental group (EG - bilateral excision of first gill arch) were submitted to graded hypoxia, with and without access to air. The first pair of gill arches ablation reduced respiratory surface area and removed innervation by cranial nerve IX. In graded hypoxia without access to air, both groups displayed bradycardia and increased ventilatory stroke volume (VT), and the IG showed a significant increase in breathing frequency (fR). The EG exhibited very high fR in normoxia that did not increase further in hypoxia, this was linked to reduced O2 extraction from the ventilatory current (EO2) and a significantly higher critical O2 tension (PcO2) than the IG. In hypoxia with access to air only the IG showed increased air-breathing, indicating that the first pair of gill arches excision severely attenuated air-breathing responses. Both groups exhibited bradycardia before and tachycardia after air-breaths. The fH and gill ventilation amplitude (VAMP) in the EG were overall higher than the IG. External and internal NaCN injections revealed that O2 chemoreceptors mediating ventilatory hypoxic responses (fR and VT) are internally oriented. The NaCN injections indicated that fR responses were mediated by receptors predominantly in the first pair of gill arches but VT responses by receptors on all gill arches. Receptors eliciting cardiac responses were both internally and externally oriented and distributed on all gill arches or extra-branchially. Air-breathing responses were predominantly mediated by receptors in the first pair of gill arches. In conclusion, the role of the first pair of gill arches is related to: a) an elevated EO2 providing an adequate O2 uptake to maintain the aerobic metabolism during normoxia; b) a significant bradycardia and increased fAB elicited by O2 chemoreceptors externally oriented; c) increase in the ventilatory variables (fR and VAMP) stimulated by O2 chemoreceptors internally oriented. Copyright © 2015 Elsevier Inc. All rights reserved.
    Full-text · Article · May 2015 · Comparative biochemistry and physiology. Part A, Molecular & integrative physiology
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    • "Hoplias malabaricus possess chemoreceptors modulating the f H responses that are internally oriented, located exclusively in the first gill arch (Sundin et al., 1999). Moreover, C. macropomum (Sundin et al., 2000), M. cephalus (Shingles et al., 2005), P. mesopotamicus (Leite et al., 2007), H. lacerdae (Micheli-Campbell et al., 2009) and H. unitaeniatus (Lopes et al., 2010), exhibit internally and externally oriented chemoreceptors distributed over all gill arches, that elicit reflex bradycardia. The attenuated bradycardia in the NaCN-opr is similar to responses observed in the catfish, Ictalurus punctatus (Burleson and Smatresk, 1990) and after external NaCN injections in P. mesopotamicus (Leite et al., 2007), both with the first pair of gill arches denervated. "
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    ABSTRACT: This study examined the distribution and orientation of gill O2 chemoreceptors in Oreochromis niloticus and their role in cardiorespiratory responses to graded hypoxia. Intact fish, and a group with the first gill arch excised (operated), were submitted to graded hypoxia and their cardiorespiratory responses (oxygen uptake - V˙O2, breathing frequency - fR, ventilatory stroke volume - VT, gill ventilation - V˙G, O2 extraction from the ventilatory current - EO2, and heart rate - fH) were compared. Their responses to bolus injections of NaCN into the bloodstream (internal) or ventilatory water stream (external) were also determined. The V˙O2 of operated fish was significantly lower at the deepest levels of hypoxia. Neither reflex bradycardia nor ventilatory responses were completely abolished by bilateral excision of the first gill arch. EO2 of the operated group was consistently lower than the intact group. The responses to internal and external NaCN included transient decreases in fH and increases in fR and Vamp (ventilation amplitude). These cardiorespiratory responses were attenuated but not abolished in the operated group, indicating that chemoreceptors are not restricted to the first gill arch, and are sensitive to oxygen levels in both blood and water.
    Preview · Article · May 2013 · Comparative biochemistry and physiology. Part A, Molecular & integrative physiology
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    • "gill ventilation (Hedrick et al., 1994). Furthermore, it suggests that the internal threshold for triggering air breaths is higher than that which triggers increases in gill ventilation, which is similar to what has been found in H . unitaeniatus (Lopes et al., 2010). "
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    ABSTRACT: This study examined mechanisms underlying cardio-respiratory acclimation to moderate sustained hypoxia (6·0 kPa for 7 days at 22° C) in the bowfin Amia calva, a facultative air-breathing fish. This level of hypoxia is slightly below the critical oxygen tension (pcrit) of A. calva denied access to air (mean ± s.e. = 9·3 ± 1·0 kPa). Before exposure to sustained hypoxia, A. calva with access to air increased air-breathing frequency on exposure to acute progressive hypoxia while A. calva without access to air increased gill-breathing frequency. Exposure to sustained hypoxia increased the gill ventilation response to acute progressive hypoxia in A. calva without access to air, regardless of whether they had access to air or not during the sustained hypoxia. Additionally, there was a decrease in Hb–O2 binding affinity in these fish. This suggests that, in A. calva, acclimation to hypoxia elicits changes that increase oxygen delivery to the gas exchange surface for oxygen uptake and reduce haemoglobin affinity to enhance oxygen delivery to the tissues.
    Full-text · Article · Jan 2013 · Journal of Fish Biology
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