Abstract
Cardiorespiratory adjustments that occur after feeding are essential to supply the demands of digestion in vertebrates. The well-documented postprandial tachycardia is triggered by an increase in adrenergic activity and by non-adrenergic non-cholinergic (NANC) factors in mammals and crocodilians, while it is linked to a withdrawal of vagal drive and NANC factors in non-crocodilian ectotherms—except for fish, in which the sole investigation available indicated no participation of NANC factors. On the other hand, postprandial ventilatory adjustments vary widely among air-breathing vertebrates, with different species exhibiting hyperventilation, hypoventilation, or even no changes at all. Regarding fish, which live in an environment with low oxygen capacitance that requires great ventilatory effort for oxygen uptake, data on the ventilatory consequences of feeding are also scarce. Thus, the present study sought to investigate the postprandial cardiorespiratory adjustments and the mediation of digestion-associated tachycardia in the unimodal water-breathing teleost Oreochromis niloticus. Heart rate (fH), cardiac autonomic tones, ventilation rate (fV), ventilation amplitude, total ventilation and fH/fV variability were assessed both in fasting and digesting animals under untreated condition, as well as after muscarinic cholinergic blockade with atropine and double autonomic blockade with atropine and propranolol. The results revealed that digestion was associated with marked tachycardia in O. niloticus, determined by a reduction in cardiac parasympathetic activity and by circulating NANC factors—the first time such positive chronotropes were detected in digesting fish. Unexpectedly, postprandial ventilatory alterations were not observed, although digestion triggered mechanisms that were presumed to increase oxygen uptake, such as cardiorespiratory synchrony.
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All data are available at https://doi.org/10.17605/OSF.IO/W685M.
References
Acheson K, Jequier E, Wahren J (1983) Influence of β-adrenergic blockade on glucose-induced thermogenesis in man. J Clin Invest 72:981–986
Altimiras J (1999) Understanding autonomic sympathovagal balance from short-term heart rate variations. Are we analyzing noise? Comp Biochem Physiol 124A:447–460
Altimiras J, Aissaoui A, Tort L, Axelsson M (1997) Cholinergic and adrenergic tones in the control of heart rate in teleosts. How should they be calculated? Comp Biochem Physiol 118A:131–139
Andrade DV, Toledo LF, Abe AS, Wang T (2004) Ventilatory compensation of the alkaline tide during digestion in the snake Boa constrictor. J Exp Biol 207:1379–1385
Andrade DV, Cruz-Neto AP, Abe AS, Wang T (2005) Specific dynamic action in ectothermic vertebrates: a review of the determinants of postprandial metabolic response in fishes, amphibians, and reptiles. In: Starck JM, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates, 1st edn. Science Publishers, Enfield, pp 305–324
Armelin VA, Braga VHS, Teixeira MT, Rantin FT, Florindo LH, Kalinin AL (2016) Gill denervation eliminates the barostatic reflex in a neotropical teleost, the tambaqui (Colossoma macropomum). Fish Physiol Biochem 42:1213–1224
Armelin VA, Thomsen MT, Teixeira MT, Florindo LH, Bayley M, Wang T (2019a) Cardiovascular and ventilatory interactions in the facultative air-breathing teleost Pangasianodon hypophthalmus. J Comp Physiol 189B:425–440
Armelin VA, Braga VHS, Guagnoni IN, Crestani AM, Abe AS, Florindo LH (2019b) Autonomic control of cardiovascular adjustments associated with orthostasis in the scansorial snake Boa constrictor. J Exp Biol 222:j197848
Ask JA (1983) Comparative aspects of adrenergic receptors in the hearts of lower vertebrates. Comp Biochem Physiol 76A:543–552
Astrup A, Simonsen L, Bülow J, Madsen J, Christensen NJ (1989) Epinephrine mediates facultative carbohydrate-induced thermogenesis in human skeletal muscle. Am J Physiol 257:E340–E345
Axelsson M, Thorarensen H, Nilsson S, Farrell AP (2000) Gastrointestinal blood flow in the red Irish lord, Hemilepidotus hemilepidotus: long-term effects of feeding and adrenergic control. J Comp Physiol 170B:145–152
Baron AD (1994) Hemodynamic actions of insulin. Am J Physiol 267:E187–E202
Braga VHS, Armelin VA, Teixeira MT, Abe AS, Rantin FT, Florindo LH (2016) The effects of feeding on cardiac control of the Broad-Nosed Caiman (Caiman latirostris): the role of the autonomic nervous system and NANC factors. J Exp Zool 325A:524–531
Bucking C, Wood CM (2008) The alkaline tide and ammonia excretion after voluntary feeding in freshwater rainbow trout. J Exp Biol 211:2533–2541
Busk M, Overgaard J, Hicks JW, Bennett AF, Wang T (2000) Effects of feeding on arterial blood gases in the American alligator Alligator mississippiensis. J Exp Biol 203:3117–3124
Campbell HA, Taylor EW, Egginton S (2004) The use of power spectral analysis to determine cardiorespiratory control in the short-horned sculpin Myoxocephalus scorpius. J Exp Biol 207:1969–1976
Campbell HA, Taylor EW, Egginton S (2005) Does respiratory sinus arrhythmia occur in fishes? Biol Lett 1:484–487
Campbell HA, Leite CAC, Wang T, Skals M, Abe AS, Egginton S, Rantin FT, Bishop CM, Taylor EW (2006) Evidence for a respiratory component, similar to mammalian respiratory sinus arrhythmia, in the heart rate variability signal from the rattlesnake, Crotalus durissus terrificus. J Exp Biol 209:2628–2636
Claësson D, Abe AS, Wang T (2015) Autonomic regulation of heart rate during specific dynamic action associated with digestion in the bullfrog Lithobates catesbeianus. Zoologia 32:492–496
Cooper CA, Wilson RW (2008) Post-prandial alkaline tide in freshwater rainbow trout: effects of meal anticipation on recovery from acid-base and ion regulatory disturbances. J Exp Biol 211:2542–2550
Costa MJ, Rivaroli L, Rantin FT, Kalinin AL (2000) Cardiac tissue function of the teleost fish Oreochromis niloticus under different thermal conditions. J Therm Biol 25:373–379
De Vera L, Rial RV, Pereda E, González JJ (2012) Autonomic mediation of the interdependence between variability signals of heart rate and blood pressure in the lizard Gallotia galloti. Can J Zool 90:839–848
DeFronzo RA, Thorin D, Felber JP, Simonson DC, Thiebaud D, Jequier E, Golay A (1984) Effect of beta and alpha adrenergic blockade on glucose-induced thermogenesis in man. J Clin Invest 73:633–639
Dejour P (1978) Carbon dioxide in water- and air-breathers. Respir Physiol 33:121–128
Diamond P, LeBlanc J (1987) Role of autonomic nervous system in postprandial thermogenesis in dogs. Am J Physiol 252:E719–E726
Donald J, Campbell G (1982) A comparative study of the adrenergic innervation of the teleost heart. J Comp Physiol 147B:85–91
Dupont-Prinet A, Claireaux G, McKenzie DJ (2009) Effects of feeding and hypoxia on cardiac performance and gastrointestinal blood flow during critical speed swimming in the sea bass Dicentrarchus labrax. Comp Biochem Physiol 154A:233–240
Enok S, Simonsen LS, Pedersen SV, Wang T, Skovgaard N (2012) Humoral regulation of heart rate during digestion in pythons (Python molurus and Python regius). Am J Physiol 302:R1176–R1183
Farrell AP (2007) Tribute to P. L. Lutz: a message from the heart—why hypoxic bradycardia in fishes? J Exp Biol 210:1715–1725
Farrell AP, Smith FM (2017) Heart physiology and function. In: Farrell AP, Brauner CJ, Hoar WS, Randall DJ (eds) The cardiovascular system: morphology, control and function, 1st edn. Elsevier, London, pp 155–264
Florindo LH, Armelin VA, McKenzie DJ, Rantin FT (2018) Control of air-breathing in fishes: central and peripheral receptors. Acta Histochem 120:642–653
Gibbins I (1994) Comparative anatomy and evolution of the autonomic nervous system. In: Nilsson S, Holgrem S (eds) Comparative physiology and evolution of the autonomic nervous system, 1st edn. Harwood Academic Publishers, London, pp 1–68
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 39:143–149
Hicks JW, Wang T, Bennett AF (2000) Patterns of cardiovascular and ventilatory response to elevated metabolic states in the lizard Varanus exanthematicus. J Exp Biol 203:2437–2445
Holeton GF, Randall DJ (1967) Changes in blood pressure in the rainbow trout during hypoxia. J Exp Biol 46:297–305
Hughes GM, Shelton G (1962) Respiratory mechanisms and their nervous control in fish. Adv Comp Physiol Biochem 1:275–364
Iversen NK, Dupont-Prinet A, Findorf I, McKenzie DJ, Wang T (2010) Autonomic regulation of the heart during digestion and aerobic swimming in the European sea bass (Dicentrarchus labrax). Comp Biochem Physiol 156A:463–468
Jobling M (1981) The influences of feeding on the metabolic rate of fishes: a short review. J Fish Biol 18:385–400
Kågstrom J, Olsson C, Axelsson M, Franklin CE (1998) Peptidergic control of gastrointestinal blood flow in the estuarine crocodile, Crocodilus porosus. Am J Physiol 274:R1740–R1750
Kalinin AL, Glass ML, Rantin FT (1999) A comparison of directly measured and estimated gill ventilation in the Nile tilapia, Oreochromis niloticus. Comp Biochem Physiol 122A:207–211
Kelbæk H, Munck O, Christensen NJ, Godtfredsen J (1989) Central haemodynamic changes after a meal. Br Heart J 61:506–509
Laurent P, Holmgren S, Nilsson S (1983) Nervous and humoral control of the fish heart: structure and function. Comp Biochem Physiol 76A:525–542
Lefevre S, Huong DTT, Phuong NT, Wang T, Bayley M (2012) Effects of hypoxia on the partitioning of oxygen uptake and the rise in metabolism during digestion in the air-breathing fish Channa striata. Aquaculture 364–365:137–142
Leite CAC, Taylor EW, Guerra CDR, Florindo LH, Belão T, Rantin FT (2009) The role of the vagus nerve in the generation of cardiorespiratory interactions in a neotropical fish, the pacu, Piaractus mesopotamicus. J Comp Physiol 195A:721–731
Li M, Hu J, Chen Z, Meng J, Wang H, Ma H, Luo X (2006) Evidence for histamine as a neurotransmitter in the cardiac sympathetic nervous system. Am J Physiol 291:H45–H51
Lopes IG, Armelin VA, Braga VHS, Florindo LH (2017) The influence of midazolam on heart rate arises from cardiac autonomic tones alterations in Burmese pythons, Python molurus. Auton Neurosci 208:103–112
Mamun SM, Focken U, Becker K (2007) Comparison of metabolic rates and feed nutrient digestibility in conventional, genetically improved (GIFT) and genetically male (GMNT) Nile tilapia, Oreochromis niloticus (L.). Comp Biochem Physiol 148A:214–222
Maricondi-Massari M, Kalinin AL, Glass ML, Rantin FT (1998) The effects of temperature on oxygen uptake, gill ventilation and ECG waveforms in the Nile tilapia, Oreochromis niloticus. J Therm Biol 23:283–290
Martins ND, Colvara WA, Rantin FT, Kalinin AL (2011) Microcystin-LR: how it affects the cardio-respiratory responses to hypoxia in Nile tilapia, Oreochromis niloticus. Chemosphere 84:154–159
McCue MD (2006) Specific dynamic action: a century of investigation. Comp Biochem Physiol 144A:381–394
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
Millidine KJ, Metcalfe NB, Armstrong JD (2008) The use of ventilation frequency as an accurate indicator of metabolic rate in juvenile Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 65:2081–2087
Monteiro DA, Taylor EW, Sartori MR, Cruz AL, Rantin FT, Leite CAC (2018) Cardiorespiratory interactions previously identified as mammalian are present in the primitive lungfish. Sci Adv 4:e0800
Nilsson S (1983) Neurotransmission. In: Nilsson S (ed) Autonomic nerve function in the vertebrates, 1st edn. Springer-Verlag, Heidelberg, pp 41–67
Nilsson S (1986) Control of gill blood flow. In: Nilsson S, Holmgren S (eds) Fish physiology: recent advances, 1st edn. Springer, Dordrecht, pp 86–101
Nilsson S, Sundin L (1998) Gill blood flow control. Comp Biochem Physiol 119A:137–147
Niv Y, Fraser GM (2002) The alkaline tide phenomenon. J Clin Gastroenterol 35:5–8
Perry SF, Wood CM (1989) Control and coordination of gas transfer in fishes. Can J Zool 67:2961–2970
Perry SF, Gilmour KM (2006) Acid–base balance and CO2 excretion in fish: unanswered questions and emerging models. Respir Physiol Neurobiol 154:199–215
Pettersson K, Nilsson S (1979) Nervous control of the branchial vascular resistance of the Atlantic cod, Gadus morhua. J Comp Physiol 129B:179–183
Reid SG, Sundin L, Florindo LH, Rantin FT, Milsom WK (2003) Effects of afferent input on the breathing pattern continuum in the tambaqui (Colossoma macropomum). Respir Physiol Neurobiol 136:39–53
Rigel DF (1988) Effects of neuropeptides on heart rate in dogs: comparison of VIP, PHI, NPY, CGRP, and NT. Am J Physiol 255:H311–H317
Ross LG, McKinney RW, Cardwell SK, Fullarton JG, Roberts SEJ, Ross B (1992) The effects of dietary protein content, lipid content and ration level on oxygen consumption and specific dynamic action in Oreochromis niloticus L. Comp Biochem Physiol 103A:573–578
Rothwell NJ, Saville ME, Stock MJ (1982) Sympathetic and thyroid influences on metabolic rate in fed, fasted, and refed rats. Am J Physiol 243:R339–R346
Sanches PVW, Taylor EW, Duran LM, Cruz AL, Dias DPM, Leite CAC (2019) Respiratory sinus arrhythmia is a major component of heart rate variability in undisturbed, remotely monitored rattlesnakes Crotalus durissus. J Exp Biol 222:jeb197954
Secor SM (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol 179B:1–56
Secor SM, White SE (2010) Prioritizing blood flow: cardiovascular performance in response to the competing demands of locomotion and digestion for the Burmese python, Python molurus. J Exp Biol 213:78–88
Secor SM, Hicks JW, Bennett AF (2000) Ventilatory and cardiovascular responses of a python (Python molurus) to exercise and digestion. J Exp Biol 203:2447–2454
Skovgaard N, Møller K, Gesser H, Wang T (2009) Histamine induces postprandial tachycardia through a direct effect on cardiac H2-receptors in pythons. Am J Physiol 296:R774–R785
Skovgaard N, Abe AS, Taylor EW, Wang T (2017) Cardiovascular effects of histamine in three widely diverse species of reptiles. J Comp Physiol 188B:153–162
Sundin L, Nilsson S (2002) Branchial innervation. J Exp Zool 293:232–248
Taylor EW (1992) Nervous control of the heart and cardiorespiratory interactions. In: Hoar WS, Randall DJ, Farrell AP (eds) Fish physiology, vol 12B. Academic Press, New York, pp 343–387
Taylor JR, Grosell M (2006) Feeding and osmoregulation: dual function of the marine teleost intestine. J Exp Biol 209:2939–2951
Taylor EW, Jordan D, Coote JH (1999) Central control of the cardiovascular and respiratory systems and their interactions in vertebrates. Physiol Rev 79:855–916
Taylor EW, Campbell HA, Levings JJ, Young MJ, Butler PJ, Egginton S (2006) Coupling of the respiratory rhythm in fish with activity in hypobranchial nerves and with heartbeat. Physiol Biochem Zool 79:1000–1009
Taylor JR, Whittamore JM, Wilson RW, Grosell M (2007) Postprandial acid–base balance and ion regulation in freshwater and seawater-acclimated European flounder, Platichthys flesus. J Comp Physiol 177B:597–608
Taylor EW, Leite CAC, Skovgaard N (2010) Autonomic control of cardiorespiratory interactions in fish, amphibians and reptiles. Braz J Med Biol Res 43:600–610
Taylor EW, Leite CAC, Sartori MR, Wang T, Abe AS, Crossley DA II (2014) The phylogeny and ontogeny of autonomic control of the heart and cardiorespiratory interactions in vertebrates. J Exp Biol 217:690–703
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 185B:669–676
Thomaz JM, Martins ND, Monteiro DA, Rantin FT, Kalinin AL (2009) Cardio-respiratory function and oxidative stress biomarkers in Nile tilapia exposed to the organophosphate insecticide trichlorfon (NEGUVON®). Ecotox Environ Safe 72:1413–1424
Troiano NM, Armelin VA, Braga VHS, Abe AS, Rantin FT, Florindo LH (2018) The autonomic control of upright posture tachycardia in the arboreal lizard Iguana iguana. J Exp Zool 329A:130–139
Waaler BA, Hisdal J, Ihlen H, Kjekshus J (2006) Mechanisms behind the postprandial increase in cardiac output: a clue obtained from transplanted hearts. Eur J Appl Physiol 97:516–520
Wang T, Burggren W, Nobrega E (1995) Metabolic, ventilatory, and acid-base responses associated with specific dynamic action in the toad Bufo marinus. Physiol Zool 68:192–205
Wang T, Taylor EW, Andrade D, Abe AS (2001a) Autonomic control of heart rate during forced activity and digestion in the snake Boa constrictor. J Exp Biol 204:3553–3560
Wang T, Busk M, Overgaard J (2001b) The respiratory consequences of feeding in amphibians and reptiles. Comp Biochem Physiol 128A:533–547
Wang T, Andersen JB, Hicks JW (2005) Effects of digestion on the respiratory and cardiovascular physiology of amphibians and reptiles. In: Starck JM, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates, 1st edn. Science Publishers, Enfield, pp 279–303
Wood CM, Kajimura M, Mommsen TP, Walsh PJ (2005) Alkaline tide and nitrogen conservation after feeding in an elasmobranch (Squalus acanthius). J Exp Biol 208:2693–2705
Wood CM, Schultz AG, Munger RS, Walsh PJ (2009) Using omeprazole to link the components of the post-prandial alkaline tide in the spiny dogfish, Squalus acanthias. J Exp Biol 212:684–692
Young JB, Saville E, Rothwell NJ, Stock MJ, Landsberg L (1982) Effect of diet and cold exposure on norepinephrine turnover in brown adipose tissue of the rat. J Clin Invest 69:1061–1071
Zena LA, Leite CAC, Longhini LS, Dias DMP, Silva GSF, Hartzler LK, Gargaglioni LH, Bícego KC (2017) Analysis of the respiratory component of heart rate variability in the Cururu toad Rhinella schneideri. Sci Rep 7:16119
Zeraik VM, Belão TC, Florindo LH, Kalinin AL, Rantin FT (2013) Branchial O2 chemoreceptors in Nile tilapia Oreochromis niloticus: control of cardiorespiratory function in response to hypoxia. Comp Biochem Physiol 166A:17–25
Acknowledgements
The authors would like to thank the INCT—FISC professors for their comments and suggestions on the present study, as well as the members of Florindo’s Laboratory for the assistance with animal care.
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This study was supported by the Brazilian National Council for Scientific and Technological Development (CNPq) and the São Paulo Research Foundation (FAPESP), through the Brazilian National Institute of Science and Technology in Comparative Physiology (INCT—FISC; Proc. Number 2008/57712-4). ING also received an undergraduate research fellowship from FAPESP (Proc. Number 2017/01616-6).
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The experiments conducted in the present study were approved by the UNESP/IBILCE Ethics Committee for Animal Research (Proc. 166/2017 CEUA), being in accordance with all the regulations and ethical guidelines in Brazil.
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Guagnoni, I.N., Armelin, V.A., da Silva Braga, V.H. et al. Postprandial cardiorespiratory responses and the regulation of digestion-associated tachycardia in Nile tilapia (Oreochromis niloticus). J Comp Physiol B 191, 55–67 (2021). https://doi.org/10.1007/s00360-020-01317-x
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DOI: https://doi.org/10.1007/s00360-020-01317-x