Abstract
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 PO2 ~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 μg NaCN in 0.2 mL saline) and external (buccal) injections of NaCN (500 μg NaCN in 1.0 mL water) on f R , V AMP, V TOT, P a and f H we conclude that the O2 receptors involved in eliciting changes in gill ventilation and associated cardiovascular responses are present on all gill arches and monitor the O2 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.
Similar content being viewed by others
References
Axelsson M, Fritsche R (1994) Cannulation techniques. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes. Analytical techniques. Elsevier, Amsterdam, pp 17–36
Axelsson M, Abe AS, Bicudo JEPW, Nilsson S (1989) On the cardiac control in the South American lungfish, Lepidosiren paradoxa. Comp Biochem Physiol 93A:561–565
Bamford OS (1974) Oxygen reception in the rainbow trout (Salmo gairdneri). Comp Biochem Physiol 48A:69–76
Burleson ML, Milsom WK (1993) Sensory receptors in the first gill arch of rainbow trout. Respir Physiol 93:97–110
Burleson ML, Smatresk NJ (1990a) Effects of sectioning cranial nerves IX and X on cardiovascular and ventilatory reflex responses to hypoxia and NaCN in channel catfish. J Exp Biol 154:407–420
Burleson ML, Smatresk NJ (1990b) Evidence for two oxygen-sensitive chemoreceptor loci in channel catfish, Ictalurus punctatus. Physiol Zool 63:208–221
Butler PJ, Taylor EW (1971) Response of the dogfish (Scyliorhinus canicula L.) to slowly induced and rapidly induced hypoxia. Comp Biochem Physiol 39A:307–323
Butler PJ, Taylor EW, Short S (1977) The effect of sectioning cranial nerves V, VII, IX and X on the cardiac response of the dogfish Scyliorhinus canicula to environmental hypoxia. J Exp Biol 69:233–245
Carter GS, Beadle LC (1931) The fauna of the swamps of the Paraguayan Chaco in relation to its environment, II. Respiratory adaptations in fishes. J Linn Soc Lond Zool 37:327–368
Coolidge EH, Ciuhandu CS, Milsom WK (2008) A comparative analysis of putative oxygen-sensing cells in the fish gill. J Exp Biol 211:1231–1242
Daxboeck C, Holeton GF (1978) Oxygen receptors in the rainbow trout, Salmo gairdneri. Can J Zool 56:1254–1256
Dehadrai PV, Tripathi SD (1976) Environmental and ecology of freshwater air-breathing teleosts. In: Hughes GM (ed) Respiration of amphibious vertebrates. Academic Press, London, pp 39–72
Farrell AP (1977) Cardiovascular events associated with air breathing in two teleosts, Hoplerythrinus unitaeniatus and Arapaima gigas. Can J Zool 56:953–958
Florindo LH, Leite CAC, Kalinin AL, Reid SG, Milsom WK, Rantin FT (2006) The role of branchial and orobranchial O2 chemoreceptors in the control of aquatic surface respiration in the neotropical fish tambaqui (Colossoma macropomum): progressive responses to prolonged hypoxia. J Exp Biol 209:1709–1715
Fritsche R, Nilsson S (1989) Cardiovascular responses to hypoxia in the Atlantic cod, Gadus morhua. Exp Biol 48:153–160
Fritsche R, Nilsson S (1993) Cardiovascular and ventilatory control during hypoxia. In: Rankin JC, Jensen FB (eds) Fish ecophysiology. Chapman and Hall, New York, pp 180–206
Glass ML, Ishimatsu A, Johansen K (1986) Responses of aerial ventilation to hypoxia and hypercapnia in Channa argus, an air-breathing fish. J Comp Physiol 156B:425–430
Graham JB (1997) Air-breathing fishes: evolution diversity and adaptation. Academic Press, San Diego
Hedrick MS, Jones DR (1999) Control of gill ventilation and air-breathing in the bowfin Amia calva. J Exp Biol 202:87–94
Holeton GF (1977) Constancy of arterial blood pH during CO-induced hypoxia in the rainbow trout. Can J Zool 55:1010–1013
Johansen K (1966) Air breathing in the teleost Symbranchus marmoratus. Comp Biochem Physiol 18:383–395
Johansen K, Lenfant C (1968) Respiration in the African lungfish, Protopterus aethiopicus II. Control of breathing. J Exp Biol 49:453–468
Johansen K, Hanso D, Lenfant C (1970) Respiration in the primitive air breather, Amia calva. Respir Physiol 9:162–174
Jonz MG, Nurse CA (2003) Neuroepithelial cells and associated innervation of the zebrafish gill: a confocal immunofluorescence study. J Comp Neurol 461:1–17
Jonz MG, Fearon IM, Nurse CA (2004) Neuroepithelal oxygenchemoreceptors of the zebrafish gill. J Physiol (Lond) 560:737–752
Kramer DL (1988) The behavioral ecology of air breathing by aquatic animals. Can J Zool 66:89–94
Kramer DL, Lindsey CC, Moodie GEE, Stevens ED (1978) The fishes and aquatic environment of the central Amazon basin, with particular reference to respiratory patterns. Can J Zool 56:717–729
Lahiri S, Szidon JP, Fishman AP (1970) Potential respiratory and circulatory adjustments to hypoxia in the African lungfish. Fed Proc 29:1141–1148
Laurent P, Rouzeau JD (1972) Afferent neural activity from the pseudobranch of teleost. Effects of PO2, pH, osmotic pressure and Na+ ions. Resp Physiol 14:307–331
Leite CAC, Florindo LH, Kalinin AL, Milsom WK, Rantin FT (2007) Gill chemoreceptors and cardio-respiratory reflexes in the neotropical teleost pacu, Piaractus mesopotamicus. J Comp Physiol A 193:1001–1011
McKenzie DJ, Burleson ML, Randall DJ (1991) The effects of branchial denervation and pseudobranch ablation on cardio-ventilatory control in an air-breathing fish. J Exp Biol 161:347–365
McKenzie DJ, Taylor EW, Bronzi P, Bolis CL (1995) Aspects of cardioventilatory control in the Adriatic sturgeon (Acipenser naccarii). Resp Phyisiol 100:45–53
McKenzie DJ, Campbell HA, Taylor EW, Micheli M, Rantin FT, Abe AS (2007) The autonomic control and functional significance of the changes in heart rate associated with air breathing in the jeju, Hoplerythrinus unitaeniatus. J Exp Biol 210:4224–4232
Milsom WK (1997) Control of breathing in fish: role of chemoreceptors. In: Val AL, Almeida-Val VMF, Randall DJ (eds) Physiology and biochemistry of the fishes of the amazon. INPA, Manaus, pp 359–377
Milsom WK, Brill RW (1986) Oxygen sensitive afferent information arising from the first gill arch of yellowfin tuna. Respir Physiol 66:193–203
Milsom WK, Reid SG, Rantin FT, Sundin L (2002) Extrabranchial chemoreceptors involved in respiratory reflexes in the neotropical fish Colossoma macropomum (the tambaqui). J Exp Biol 205:1765–1774
Oliveira RD, Lopes JM, Sanches JR, Kalinin AL, Glass M, Rantin FT (2004) Cardiorespiratory responses of the facultative air-breathing fish jeju, Hoplerythrinus unitaeniatus (Teleostei, Erythrinidae), exposed to graded ambient hypoxia. Comp Biochem Physiol 139A:479–485
Perry SF, Gilmour KM (2002) Sensing and transfer of respiratory gases at the fish gill. J Exp Biol 293:249–263
Randall DJ, Jones DR (1973) The effects of deafferenation of the pseudobranch on the respiratory response to hypoxia and hyperoxia in the trout (Salmo gairdneri). Respir Physiol 17:291–302
Randall DJ, Cameron JN, Daxboeck C, Smatresk N (1981) Aspects of bimodal gas exchange in the bowfin, Amia calva (Actinopterygii: Amiiformes). Respir Physiol 43:339–348
Rantin FT, Kalinin AL (1996) Cariorespiratory function and aquatic surface respiration in Colossoma macropomum exposed to graded and acute hypoxia. In: Val AL, Almeida-Val, Randall DJ (eds) Physiology and biochemistry of the fishes of the Amazon. INPA Manaus, Brazil, pp 169–180
Rantin FT, Kalinin AL, Glass ML, Fernandes MN (1992) Respiratory responses to hypoxia in relation to mode of life of two erythrinid species (Hoplias malabaricus and Hoplias lacerdae). J Fish Biol 41:805–812
Rantin FT, Guerra CDR, Kalinin AL, Glass ML (1998) The influence of aquatic surface respiration (ASR) on cardio-respiratory function of the serrasalmid fish Piaractus mesopotomicus. Comp Biochem Physiol 119(A):991–997
Reid SG, Sundin L, Milsom WK (2005) The cardio-respiratory system in tropical fish: structure, function and control. In: Val AL, Almeida-Val VMF, Randall DJ (eds) The physiology of tropical fish. Fish physiology. Elsevier Science, San Diego, pp 225–275
Riggs A, Fyhn HJ, Fyhn UEH, Noble RW (1978) Estudo das propriedades funcionais da hemoglobina de Hoplias malabaricus e Hoplerythrinus unitaeniatus. Acta Amazônica 8:251–257
Satchell GH (1961) The response of the dogfish to anoxia. J Exp Biol 38:531–543
Saunders RL, Sutterlin AM (1971) Cardiac and respiratory response to hypoxia in the searaven, Hemitripterus americanus, an investigation of possible control mechanism. J Fish Res Board Can 28:491–503
Shelton G, Jones DR, MilsomWK (1986) Control of breathing in ectotermic vertebrates. In: Geiger SR, Fishman AP, Cherniack NS, Widdicombe JG (eds) Handbook of physiology, section 3, the respiratory system, Vol II, control of breathing, part 2. Waverly Press, Baltimore, pp 857–909
Singh BN (1976) Balance between aquatic and aerial respiration. In: Hughes GM (ed) Respiration in amphibious vertebrates. Academic Press, London, pp 125–164
Skals M, Skovgaard N, Taylor EW, Leite CAC, Abe AS, Wang T (2006) Cardiovascular changes under normoxic and hypoxic conditions in the air-breathing teleost Symbranchus marmoratus: importance of the venous system. J Exp Biol 209:4167–4173
Smatresk NJ (1986) Ventilatory and cardiovascular responses to hypoxia and NaCN in Lepisosteus osseus, an air-breathing fish. Physiol Zool 59:385–397
Smatresk NJ (1988) Control of the respiratory mode in air-breathing fishes. Can J Zool 66:144–151
Smatresk NJ (1989) Chemoreflex control of respiration in an air-breathing fish. In: Lahiri S, Foster RE II, Davies RO, Pack AI (eds) Chemoreceptors and chemoreflexes in breathing—cellular and molecular aspects. Oxford University Press, London, pp 29–52
Smatresk NJ, Cameron JN (1982) Respiration and acid-base physiology of the spotted gar, a bimodal breather. III. Response to a transfer from fresh water to 50% sea water, and control of ventilation. J Exp Biol 96:295–306
Smatresk NJ, Burleson ML, Azizi SQ (1986) Chemoreflexive responses to hypoxia and NaCN in longnose gar: evidence for two chemoreceptive loci. Am J Physiol 251:116–125
Smith FM, Davie PS (1984) Effects of sectioning cranial nerves IX and X on the cardiac response to hypoxia in the coho salmon, Oncorhynchus kisutch. Can J Zool 62:766–768
Smith FM, Jones DR (1978) Localization of receptors causing hypoxic bradycardia in trout (Salmo gairdneri). Can J Zool 56:1260–1265
Stevens ED, Holeton GF (1978) The partitioning of oxygen uptake from air and from water by erythrinids. Can J Zool 56:965–969
Sundin L, Nilsson G (1997) Neurochemical mechanisms behind gill microcirculatory responses to hypoxia in trout: in vivo microscopy study. Am J Physiol 272:576–585
Sundin L, Reid SG, Kalinin AL, Rantin FT, Milsom WK (1999) Cardiovascular and respiratory reflexes: the tropical fish, traira (Hoplias malabaricus) O2 chemoresponses. Respir Physiol 116:181–199
Sundin L, Reid SG, Rantin FT, Milsom WK (2000) Branchial receptors and cardio-respiratory reflexes in a neotropical fish, the tambaqui (Colossoma macropomum). J Exp Biol 203:1225–1239
Acknowledgments
This study was supported by the São Paulo State Research Foundation, FAPESP, and the Brazilian National Research Council for Development of Sciences and Technology, CNPq (grants to Tadeu Rantin) and NSERC of Canada (grants to William. K. Milsom). We would like to thank Cosima Ciuhandu (Department of Zoology/UBC) and Tiago de Campos Belão (Department of Physiological Sciences/UFSCar) for their excellent assistance with these experiments.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by G. Heldmaier.
Rights and permissions
About this article
Cite this article
Lopes, J.M., de Lima Boijink, C., Florindo, L.H. et al. Hypoxic cardiorespiratory reflexes in the facultative air-breathing fish jeju (Hoplerythrinus unitaeniatus): role of branchial O2 chemoreceptors. J Comp Physiol B 180, 797–811 (2010). https://doi.org/10.1007/s00360-010-0461-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-010-0461-2