Abstract
We examined the cardiorespiratory responses to 6 h of acute hypercarbia (1, 2.5, and 5% CO2) in intact and gill-denervated (bilateral denervation of branchial branches of cranial nerves IX and X) tambaqui, Colossoma macropomum. Intact fish exposed to 1 and 2.5% CO2 increased respiratory frequency (f R) and ventilation amplitude (V AMP) slowly over a 1- to 3-h period. Denervated fish did not show this response, suggesting that tambaqui possess receptors in the gills that will produce excitatory responses to low levels of hypercarbia (1 and 2.5% CO2) if the exposure is prolonged. The cardiac response to stimulation of these receptors with this level of CO2 was a tachycardia and not a bradycardia. During exposure to 5% CO2, intact fish increased f R and V AMP, and showed a pronounced bradycardia after 1 h. After 2 h, the heart rate (f H) started to increase, but returned to control values after 6 h. In denervated fish, the increase in f R was abolished. The slow increase in V AMP and the bradycardia were not abolished, suggesting that these changes arose from extra-branchial receptors. Neither intact nor denervated fish developed the swelling of the lower lip or performed aquatic surface respiration, even after 6 h, suggesting that these are unique responses to hypoxia and not hypercarbia.
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Abbreviations
- ASR:
-
aquatic surface respiration
- f H :
-
heart frequency
- f R :
-
respiratory frequency
- V AMP :
-
ventilation amplitude
- V̇ TOT :
-
total ventilation
References
Burleson ML, Smatresk NJ, Milsom WK (1992) Afferent inputs associated with cardioventilatory control in fish. In: Hoar WS, Randall DJ, Farrell AP (eds) Fish physiology: the cardiovascular system. vol 12B. Academic Press, New York, pp 389–426
Butler PJ, Taylor EW (1971) Response of the dogfish (Scyliorhinus canicula L.) to slowly induced and rapidly induced hypoxia. Comp Biochem Physiol A 39:307–323
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
Gilmour KM (2001) The CO2/pH ventilatory drive in fish. Comp Biochem Physiol A 130:219–40
Gilmour KM, Perry SF (1994) The effects of hypoxia, hyperoxia or hypercapnia on acid–base disequilibrium in the arterial blood of rainbow trout. J Exp Biol 192:269–284
Glass ML, Rantin FT, Verzola RMM, Fernandes MN, Kalinin AL (1991) Cardio-respiratory synchronization and myocardial function in hypoxic carp, Cyprinus carpio L. J Fish Biol 39:142–149
Heisler N, Towes DP, Holeton GF (1988) Regulation of ventilation and acid–base status in the elasmobranch Scyliorhinus stellaris during hyperoxia induced hypercapnia. Resp Physiol 71:227–246
Janssen RG, Randall DJ (1975) The effects of changes in pH and PCO2 in blood and water on breathing in rainbow trout, Salmo gairdneri. Resp Physiol 25:235–245
Kinkead R, Perry SF (1991)The effects of catecholamines on ventilation in rainbow trout during hypoxia or hypercapnia. Resp Physiol 84:77–92
Kramer DL (1983) The evolutionary ecology of respiratory mode in fishes: an analysis based on the costs of breathing. Environ Biol Fish 9:145–158
McKendry JE (2000) CO2 chemoreception and cardiovascular effects of hypercarbia in fish. MSc Thesis, University of Ottawa, Canada
McKendry JE, Perry SF (2001) Cardiovascular effects of hypercarbia in rainbow trout (Oncorhynchus mykiss): a role for externally oriented chemoreceptors. J Exp Biol 204:115–125
Milsom WK, Sundin L, Reid SG, Kalinin AL, Rantin FT (1999) Chemoreceptor control of cardiovascular reflexes. In: Val AL, Almeida-Val VMF (eds) Biology of tropical fishes. Editora do INPA, Manaus, pp 363–374
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
Perry SF, Wood CM (1989) Control and coordination of gas transfer in fish. Can J Zool 67:2961–2970
Perry SF, Kinkead R, Fritche R (1992) Are circulating catecholamines involved in the control of breathing by fishes? Rev Fish Biol Fish 2:65–83
Perry SF, McKendry JE (2001) The relative roles of external and internal CO2 versus H(+) in eliciting the cardiorespiratory responses of Salmo salar and Squalus acanthias to hypercarbia. J Exp Biol 204:3963–3971
Randall DJ (1990) Control and co-ordination of gas exchange in water breathers. In: Boutilier RG (ed) Advances in comparative and environmental physiology: vertebrate gas exchange from environment to cell. vol 6. Springer, Berlin Heidelberg New York, pp 253–278
Randall DJ, Taylor EW (1991) Evidence of a role for catecholamines in the control of breathing in fish. Rev Fish Biol Fish 1:139–157
Rantin, FT, Kalinin, AL (1998) The influence of aquatic surface respiration (ASR) on cardio-respiratory function of the serrasalmid fish Piaractus mesopotamicus. Comp Biochem Physiol A 119:991–997
Rantin FT, Kalinin AL (1996) Cardiorespiratory function and aquatic surface respiration in Colossoma macropomum exposed to graded and acute hypoxia. In: Val AL, Almeida-Val VMF, Randall DJ (eds) Physiology and biochemistry of the fishes of the Amazon. Editora do INPA, Manaus, pp 169–180
Reid SG, Bernier NJ, Perry SG (1998) The adrenergic stress response in fish. Control of catecholamine storage and release. Comp Biochem Physiol C 120:1–27
Reid SG, Sundin L, Kalinin AL, Rantin FT, Milsom WK (2000) Cardiovascular and respiratory reflexes in the tropical fish, traíra (Hoplias malabaricus): CO2/pH chemoreceptors. Resp Physiol 120:47–59
Saint-Paul U (1988) Diurnal routine O2 consumption at different O2 concentration by Colossoma macropomum and Colossoma brachypomum (Teleostei, Serrasalmidae). Comp Biochem Physiol 89:675–682
Smatresk NJ (1990) Chemoreceptor modulation of endogenous respiratory rhythms in vertebrates. Am J Physiol 259:R887–R897
Smith FM, Jones DR (1982) The effect of changes in blood oxygen-carrying capacity on ventilation volume in the rainbow trout (Salmo gairdneri). J Exp Biol 97:325–334
Sundin L, Reid SG, Kalinin AL, Rantin FT, Milsom WK (1999) Cardiovascular and respiratory reflexes: the tropical fish traíra (Hoplias malabaricus) O2 chemoresponses. Resp Physiol 116:181–199
Sundin L, Reid SG, Rantin FT, Milsom WK (2000) Branchial receptors and cardiorespiratory reflexes in a neotropical fish, the tambaqui (Colossoma macropomum). J Exp Biol 203:1225–1239
Thomas BL, LeRuz H (1982). A continuous study of rapid changes in blood acid–base status of trout during variations of water PCO2. J Comp Physiol 148:123–130
Val AL, Almeida-Val VMF (1995) Fishes of the Amazon and their environment. physiological and biochemical features. Springer, Berlin Heidelberg New York
Wood CM, Turner JD, Munger Graham MS (1990) Control of ventilation in the hypercarbic skate Raja ocellata. Resp Physiol 80:279–297
Acknowledgements
This study was supported by FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo, SP, Brazil—Procs. 98/13112-0, 98/13534-1), CNPq (Brazilian National Research Council for Development of Sciences and Technology—PhD fellowship to L.H.F.), and the NSERC (Natural Sciences and Engineering Research Council) of Canada (scientific and operating grants to W.K.M.). The authors also would like to acknowledge CAUNESP/Jaboticabal, SP, for providing the fish. The experiments of the present study comply with the current Brazilian laws for animal experimentation.
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Florindo, L.H., Reid, S.G., Kalinin, A.L. et al. Cardiorespiratory reflexes and aquatic surface respiration in the neotropical fish tambaqui (Colossoma macropomum): acute responses to hypercarbia. J Comp Physiol B 174, 319–328 (2004). https://doi.org/10.1007/s00360-004-0417-5
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DOI: https://doi.org/10.1007/s00360-004-0417-5