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Ventilatory responses of the clown knifefish, Chitala ornata, to hypercarbia and hypercapnia

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Abstract

The aim of the present study was to determine the roles of externally versus internally oriented CO2/H+-sensitive chemoreceptors in promoting cardiorespiratory responses to environmental hypercarbia in the facultative air-breathing fish, Chitala ornata (the clown knifefish). Fish were exposed to environmental acidosis (pH ~ 6.0) or hypercarbia (≈ 30 torr PCO2) that produced changes in water pH equal to the pH levels of the acidotic water to distinguish the relative roles of CO2 versus H+. We also injected acetazolamide to elevate arterial levels of PCO2 and [H+] in fish in normocarbic water to distinguish between internal and external stimuli. We measured changes in gill ventilation frequency, air breathing frequency, heart rate and arterial blood pressure in response to each treatment as well as the changes produced in arterial PCO2 and pH. Exposure to normocarbic water of pH 6.0 for 1 h did not produce significant changes in any measured variable. Exposure to hypercarbic water dramatically increased air breathing frequency, but had no effect on gill ventilation. Hypercarbia also produced a modest bradycardia and fall in arterial blood pressure. Injection of acetazolamide produced similar effects. Both hypercarbia and acetazolamide led to increases in arterial PCO2 and falls in arterial pH although the changes in arterial PCO2/pH were more modest following acetazolamide injection as were the increases in air breathing frequency. The acetazolamide results suggest that the stimulation of air breathing was due, at least in part, to stimulation of internally oriented CO2/H+ chemoreceptors monitoring blood gas changes.

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References

  • Aota S, Holmgren KD, Gallaugher P, Randall DJ (1990) A possible role for catecholamines in the ventilatory responses associated with internal acidosis or external hypoxia in rainbow trout. J Exp Biol 151:57–70

    CAS  Google Scholar 

  • Babiker MM (1979) Respiratory behaviour, oxygen consumption and relative dependence on aerial respiration in the African lungfish (Protopterus anectens, Owen) and an air breathing teleost (Clarius lazera, C.). Hydrobiologia 65:177–187

    Article  Google Scholar 

  • Belão TC, Zeraik VM, Florindo LH, Kalinin AL, Leite CAC, Rantin FT (2011) Control of cardiorespiratory function in response to hypoxia in an air-breathing fish, the African catfish, Clarias gariepinus. Comp Biochem Physiol A 187:130–140

    Article  CAS  Google Scholar 

  • Belão TC, Leite CAC, Florindo LH, Kalinin AL, Rantin FT (2015) Cardiorespiratory responses to hypoxia in the African catfish, Clarias gariepinus (Burchell 1822), an air-breathing fish. J Comp Physiol B 181:905–916

    Article  CAS  Google Scholar 

  • Corcoran AE, Wilson RJA, Harris MB (2007) Central CO2/pH chemosensitivity in a modern air-breathing teleost; evidence in vitro and in vivo. Soc Neurosci Abstr 297:11

    Google Scholar 

  • Damsgaard C, Gam LTH, Tuong DD, Thinh PV, Huong DTT, Wang T, Bayley M (2015) High capacity for extracellular acid–base regulation in the air-brething fish Pangasianodon hypophthalmus. J Exp Biol 218:1290–1294

    Article  PubMed  Google Scholar 

  • de Lima Bojink CL, Florindo LH, Leite CAC, Kalinin AL, Milsom WK, Rantin FT (2010) Hypercarbic cardiorespiratory reflexes in the facultative air-breathing fish jeju (Hoplerythrinus unitaeniatus): role of branchial CO2 chemoreceptors. J Exp Biol 213:2792–2807

    Google Scholar 

  • Dehadrai PV (1962) Respiratory function of the swimbladder of Notopteru (Lacépède). Paper presented at the Proceedings of the Zoological Society of London

  • Delaney RG, Lahiri S, Fishman AP (1974) Aestivation of the African lungfish Protopterus aethiopicus: cardiovascular and respiratory functions. J Exp Biol 61:111–128

    PubMed  CAS  Google Scholar 

  • Delaney RG, Shub C, Fishman AP (1976) Haematologic observations on the aquatic and aestivating African lungfish Protopterus aethiopicus. Copeia 1976:423–434

  • Delaney RG, Lahiri S, Hamilton R, Fishman AP (1977) Acid–base balance and plasma composition in the aestivating lungfish (Protopterus). Am J Physiol 232:R10–R17

    PubMed  CAS  Google Scholar 

  • Gilmour KM (2001) The CO2/pH ventilatory drive in fish. Comp Biochem Physiol A 130:219–240

    Article  CAS  Google Scholar 

  • Gilmour KM, Milsom WK, Rantin FT, Reid SG, Perry SF (2005) Cardiorespiratory responses to hypercarbia in tambaqui Colossoma macropomum: chemoreceptor orientation and specificity. J Exp Biol 208(6):1095–1107

    Article  PubMed  CAS  Google Scholar 

  • Graham JB (1997) Air-breathing fishes: evolution, diversity, and adaptation. Academic Press, San Diego

    Google Scholar 

  • Graham JB, Baird TA (1982) The transition to air breathing in fishes: I. environmental effects on the facultative air breathing of Ancistrus chagresi and Hypostomus plecostomus (Loricariidae). J Exp Biol 96:53–67

    Google Scholar 

  • Graham MS, Turner JD, Wood CM (1990) Control of ventilation in the hypercapnic skate, Raja ocellata. I. Blood and extradural fluid chemistry. Respir Physiol 80:259–277

    Article  PubMed  CAS  Google Scholar 

  • Harter TS, Shartau RB, Brauner CJ and Farrell AP (2014) Validation of the i-STAT system for the analysis of blood parameters in fish. Conserv Physiol 2. https://doi.org/10.1093/conphys/cou037

  • Hedrick MS, Burleson ML, Jones DR, Milsom WK (1991) An examination of central chemosensitivity in an air-breathing fish (Amia calva). J Exp Biol 155:165–174

    Google Scholar 

  • Heisler N, Toews DP, Holeton GF (1988) Regulation of ventilation and acid–base status in the elasmobranch Scyliorhinus stellaris during hyperoxia induced hypercapnia. Respir Physiol 71:227–246

    Article  PubMed  CAS  Google Scholar 

  • Hoffman M, Harris MB, Taylor BE (2009) Characterization and validation of aerial respiration and central CO2 chemosensitivity in the Alaska blackfish, Dallia pectoralis. FASEB J 23:598.16

    Google Scholar 

  • Iversen NK, Huong DTT, Bayley M, Wang T (2011) Autonomic control of the heart in the Asian swamp eel (Monopterus albus). Comp Biochem Physiol 158A:485–489

    Article  CAS  Google Scholar 

  • Janssen RG, Randall DJ (1975) The effects of changes in pH and PCO2 in bood and water on breathing in rainbow trout, Salmo gairdneri. Respir Physiol 25:235–245

    Article  PubMed  CAS  Google Scholar 

  • Jesse MJ, Shub C, Fishman AP (1967) Lung and gill ventilation of the African lungfish. Respir Physiol 3:267–287

    Article  PubMed  CAS  Google Scholar 

  • Johansen K (1966) Air breathing in the teleost Symbranchus marmoratus. Comp Biochem Physiol 18:383–395

    Article  PubMed  CAS  Google Scholar 

  • Johansen K, Lenfant C (1968) Respiration in the African lungfish, Protopterus aethiopicus. II. Control of breathing. J Exp Biol 49:453–468

    PubMed  CAS  Google Scholar 

  • Johansen K, Lenfant C, Grigg GC (1967) Respiratory control in the lungfish, Neoceratodus fosteri (Krefft). Comp Biochem Physiol 20:835–854

    Article  Google Scholar 

  • Johansen K, Hanson D, Lenfant C (1970) Respiration in a primitive air breather, Amia calva. Respir Physiol 9:162–174

    Article  PubMed  CAS  Google Scholar 

  • Jonz MG, Zachar PC, Da Fonte DF, Mierzwa AS (2015) Peripheral chemoreceptiors in fish: a brief history and a look ahead. Comp Biochem Physiol A 186:27–38

    Article  CAS  Google Scholar 

  • Li S, Lu X, Bush RT (2013) CO2 partial pressure and CO2 emission in the Lower Mekong River. J Hydrology 504:40–56

    Article  CAS  Google Scholar 

  • Lomholt JP, Johansen K (1974) Control of breathing in Amphipnous cuchia, an amphibious fish. Respir Physiol 21:325–340

    Article  PubMed  CAS  Google Scholar 

  • Lopes JM, Boijink CL, Florindo LH, Leite CAC, Kalinin AL, Milsom WK, Rantin FT (2010) Hypoxic cardiorespiratory reflexes in the facultative air-breathing fish jeju (Hoplerythrinus unitaeniatus): role of branchial O2 chemoreceptors. J Comp Physiol 180B:797–811

    Article  Google Scholar 

  • Malte CL, Jakobsen SL, Wang T (2014) A critical evaluation of automated blood gas measurements in comparative respiratory physiology. Comp Biochem Physiol A Mol Integr Physiol 178:7–17

    Article  PubMed  CAS  Google Scholar 

  • McKendry JE, Perry SF (2001) Cardiovascular effects of hypercapnia in rainbow trout (Oncorhynchus mykiss): a role for externally oriented chemoreceptors. J Exp Biol 204:115–125

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • McMahon BR, Burggren WW (1987) Respiratory physiology of intestinal air breathing in the teleost fish Misgurnus anguillicaudatus. J Exp Biol 133:371–393

    Google Scholar 

  • Milsom WK (2012) New insights into gill chemoreception: receptor distribution and roles in water and air breathing fish. Respir Physiol Neurobiol 184(3):326–339

    Article  PubMed  CAS  Google Scholar 

  • Perry SF, Gilmour KM (2002) Sensing and transfer of respiratory gases at the fish gill. J Exptl Zool 293:249–263

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Poulsen AF, Hortle K, Valbo-Jorgensen J, Chan S, Chhuon C, Viravong S, Nguyen T (2004) Distribution and ecology of some important riverine fish species of the Mekong River Basin. MRC Tech Paper 10:116

    Google Scholar 

  • Reid SG, Sundin L, Kalinin AL, Rantin FT, Milsom WK (2000) Cardiovascular and respiratory reflexes in the tropical fish, traíra (Hoplias malabaricus): CO2/pH chemoresponses. Respir Physiol 120:47–59

    Article  PubMed  CAS  Google Scholar 

  • Sanchez AP, Glass ML (2001) Effects of environmental hypercapnia on pulmonary ventilation of the South American lungfish. J Fish Biol 58:1181–1189

    Article  Google Scholar 

  • Sanchez AP, Hoffmann A, Rantin FT, Glass ML (2001) Relationship between cerebro-spinal fluid pH and pulmonary ventilation of the South American lungfish, Lepidosiren paradoxa (Fitz.). J Exp Zool 290:421–425

    Article  PubMed  CAS  Google Scholar 

  • Sanchez AP, Giusti H, Bassi M, Glass ML (2005) Acid–base regulation in the South American lungfish Lepidosiren paradoxa: Effects of prolonged hypercarbia on blood gases and pulmonary ventilation. Physiol Biochem Zool 78:908–915

    Article  PubMed  CAS  Google Scholar 

  • Simard E, Trepanier G, Larochelle J, Kinkead R (2003) Intermittent hypoxia and plasticity of respiratory chemoreflexes in metamorphic bullfrog tadpoles. Respir Physiol Neurobiol 135:59–72

    Article  PubMed  Google Scholar 

  • Smatresk NJ (1988) Control of the respiratory mode in air-breathing fishes. Can J Zool 66:144–151

    Article  Google Scholar 

  • Smatresk NJ, Cameron JN (1982) Respiration and acid–base physiology of the spotted gar, a bimodal breather. II. Responses to temperature change and hypercapnia. J Exp Biol 96:1253 281–293

    Google Scholar 

  • Smith HW (1930) Metabolism of the lungfish Protopterus aethiopicus. J Biol Chem 88:97–130

    CAS  Google Scholar 

  • Soivio A, Nynolm K, Westman K (1975) A technique for repeated sampling of the blood of individual resting fish. J Exp Biol 63(1):207–217

    PubMed  CAS  Google Scholar 

  • 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(7):1225–1239

    PubMed  CAS  Google Scholar 

  • Taylor EW, Leite CAC, Sartori MR, Wang T, Abe AS, Crossley DA (2014) The phylogeny and ontogeny of autonomic control of the heart and cardiorespiratory interactions in vertebrates. J Exp Biol 217:690–703

    Article  PubMed  Google Scholar 

  • Teixeira MT, Armelin VA, Abe AS, Rantin FT, Florindo LH (2015) Autonomic control of post-air-breathing tachycardia in Clarias gariepinus (Teleostei: Clariidae). J Comp Physiol B 185:669–676

    Article  PubMed  CAS  Google Scholar 

  • Thomsen M, Wang T, Milsom W, Bayley M (2017) Lactate provides a strong pH independent ventilatory signal in the facultative air-breathing teleost Pangasianodon hypopthalmus. Sci Rep 7:6378

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tuong DD, Ngoc TB, Huynh VTN, Huong DTT, Phuong NT, Hai TN, Wang T, Bayley M (2018) Clown knifefish (Chitala ornata) oxygen uptake and its partitioning in present and future temperature environments. Comp Biochem Physiol A Mol Integr Physiol. 216:52–59

  • Ultsch GR (1987) The potential role of hypercarbia in the transition from water-breathing to air-breathing in vertebrates. Evolution 41:442–445

    Article  PubMed  Google Scholar 

  • Vidthayanon C (2012) Chitala ornata. IUCN Red List Threat Species. https://doi.org/10.2305/IUCN.UK.2012-1.RLTS.T181056A1693604.en

    Article  Google Scholar 

  • Viet TV (2015) Applications of GIS for evaluation the current culture status of Clown knife fish (Chitala ornata) in Phung Hiep District, Hau Giang Province. J Can Tho Univ 38:109–115

    Google Scholar 

  • Wilson RJA, Harris MB, Remmers JE, Perry SF (2000) Evolution of air-breathing and central CO2/H+ respiratory chemosensitivity: new insights from an old fish? J Exp Biol 203:3505–3512

    PubMed  CAS  Google Scholar 

  • Wood CM, Munger RS (1994) Carbonic anhydrase injection provides evidence for the role of blood acid–base status in stimulating ventilation after exhaustive exercise in rainbow trout. J Exp Biol 194:225–253

    PubMed  CAS  Google Scholar 

  • Wood CM, Turner JD, Munger RS, Graham MS (1990) Control of ventilation in the hypercapnic skate Raja ocellata: II. Cerebrospinal fluid and intracellular pH in the brain and other tissues. Respir Physiol 80:279–298

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was funded by the Danish Ministry of Foreign Affairs: Danida fellowship Centre Project 272 number: DFC 12-014AU iAQUA, The Danish International Development Agency (DANIDA) and by the Natural Sciences and Engineering Research Council of Canada.

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Authors and Affiliations

  1. Department of Aquatic Nutrition and Products Processing, College of Aquaculture and Fisheries, Can Tho University, Can Tho, Vietnam

    Dang Diem Tuong, Do Thi Thanh Huong & Nguyen Thanh Phuong

  2. Department of Biology, McMaster University, Hamilton, Canada

    Brittney Borowiec

  3. Department of Biological Sciences, University of Alberta, Edmonton, Canada

    Alexander M. Clifford

  4. Department of Physiological Sciences, Universidade Federal de São Carlos, São Carlos, Brazil

    Renato Filogonio

  5. Department of Zoology, University of British Columbia, Vancouver, Canada

    Alexander M. Clifford, Derek Somo & William K. Milsom

  6. Department of Bioscience, Zoophysiology, Aarhus University, Aarhus, Denmark

    Tobias Wang & Mark Bayley

  7. Aarhus Institute of Advanced Studies, 8000, Aarhus C, Denmark

    Tobias Wang

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  1. Dang Diem Tuong
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  2. Brittney Borowiec
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  3. Alexander M. Clifford
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  7. Nguyen Thanh Phuong
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  10. William K. Milsom
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Correspondence to William K. Milsom.

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Communicated by G. Heldmaier.

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Tuong, D.D., Borowiec, B., Clifford, A.M. et al. Ventilatory responses of the clown knifefish, Chitala ornata, to hypercarbia and hypercapnia. J Comp Physiol B 188, 581–589 (2018). https://doi.org/10.1007/s00360-018-1150-9

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  • DOI: https://doi.org/10.1007/s00360-018-1150-9

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