Preferences help
enabled [disable] Abstract
Number of results
2010 | 59 | 3-4 | 479-496
Article title

Czy istnieją ryby, które mają płuca? Adaptacje morfologiczne i fizjologiczne ryb do warunków hipoksji i hiperoksji

Title variants
Does a fish with lungs exist? Morphological and physiological adaptations to aquatic hypoxia and hyperoxia
Languages of publication
Dissolved oxygen is one of the most important environmental factors affecting survival of fishes that rely on aquatic respiration. Fishes face an ever changing availability of environmental oxygen, resulting for instance from the dynamics of temperature changes, surface agitation, primary production by plants and algae, and oxygen consumption by plants, animals as well as chemical processes. In natural fish environment the oxygen levels exhibit a daily cycle, depletion (consumption) during the night, and production of oxygen that might lead to supersaturation levels of up to 300% during the day. At the organismal level, the lack of sufficient oxygen in environment (hypoxia) and oxygen oversaturation (hyperoxia), will result in the reaction of chemoreceptors, the respiratory response in brain, as well as in general metabolism, growth, behavior, and important morphological adaptations. In water-breathing teleost fish hypoxia induces hyperventilation, bradycardia, and results in an elevation in gill vasculatory resistance. The phenomenon of changes in the gill structure in Carassius carassius has been also described, which included lack of protruding secondary lamellae in normoxia due to complete embedding in intralamellar cell mass (ILCM). In hypoxic water a large reduction in ILCM occurred, making the lamellae to protrude and increasing the respiratory surface by about 7.5 fold. These morphological changes were found to be reversible and apparently caused by an increased apoptosis combined with reduced cell proliferation. Although, this seemed to be a plausible explanation, further studies did not unequivocally associate ILCM with normoxic conditions. Fish have also been found to adapt to extreme hypoxia or anoxia by employing alternate metabolic pathways for anaerobic energy production. Members of the genus Carassius are the only vertebrates that are known to produce energy by fermentation of glucose to ethanol and carbon dioxide. All physiological responses to hypoxia, and probably to hyperoxia, arise principally from peripheral chemoreceptors located in the gills (neuroepithelial cells, NECs). Additionally, hypoxia induced factor HIF-1α is a key transcription factor in mediating various responses to low level of oxygen. Chronic or repeated challenges elicit responses that further modify the respiratory phenotype in ways that improve and regulate oxygenation in tissues. Aquatic hypoxia has been cited as the primary driving force in the evolution of air breathing in fish. The fish from order Semionotiformes (garfishes) and Polypteriformes (Polypterus senegalus) use respiratory gas bladder (RGB) and lungs, respectively, to acquire atmospheric oxygen. These organs may confer a high degree of independence from water quality to achieve the metabolic scope for activity and the ability to recover from hypoxia. Thus, the air-breathing fish, may not only survive aquatic hypoxia but may also maintain normal levels of activity when branchial O2 uptake is limited. The evolutionary transition to air breathing has been accompanied by biochemical and morphological modifications of respiratory structures as well as altered ventilatory regulation. However, there is clearly an ontogenic aspect to this transition from unimodal gill and/or body surface respiration to bimodal, water and air respiration.
Physical description
  • Pracownia Histologii i Embriologii Kręgowców, Wydział Biologii i Nauk o Ziemi, Uniwersytet Mikołaja Kopernika w Toruniu, Gagarina 9, 87-100 Toruń, Polska
  • School of Environment and Natural Resources, Ohio State University, 2021 Coffey Rd., Columbus, OH 43210, USA, Polska
  • Acott C., 1999. Oxygen toxicity a brief history of oxygen in diving. SPUMS J. 29, 150-155.
  • Babiker M. M., 1984. Development of dependence on aerial respiration in Polypterus senegalus (Cuvier). Hydrobiologia 110, 351-363.
  • Barluenga M., Stölting K. N., Salzburger W., Muschick M., Meyer A., 2006. Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439, 719-723.
  • Barthelemy L., Belaud A., Chastel C., 1981. A comparative study of oxygen toxicity in vertebrates. Respir. Physiol. 44, 261-268.
  • Brauner C. J., 1999. The effect of diet and short duration hyperoxia exposure on seawater transfer in coho salmon smelts (Oncorhynchus kisutch). Aquaculture 177, 257-265.
  • Bavis R. W., Powell F. L., Bradford A., Hsia C. C. W., Peltonen J. E., Soliz J., Zeis B., Fergusson E. K., Fu Z., Gassmann M., Kim C. B., Maurer J., McGuire M., Miller B. M., O'Halloran K. D., Paul R. J., Reid S. G., Rusko H. K., Tikkanen H. O., Wilkinson K. A., 2006. Respiratory plasticity in response to changes in oxygen supply and demand. Integr. Comp. Biol. 47, 532-551.
  • Brauner C. J., Matey V., Wilson J. M., Bernier N. J., Val A. L., 2004. Transition in organ function during the evolution of air-breathing; insights from Arapaima gigas, an obligate air-breathing teleost from the Amazon. J. Exp. Biol. 207, 1433-1438.
  • Burleson M. L., Shipman B. N., Smatresk N. J., 1998. Ventilation and acid-base recovery following exhausting activity in an air-breathing fish. J. Exp. Biol. 20, 1359-1368.
  • Cecchini S., Saroglia M., 2002. Antibody response in sea bass (Dicentrarchus labrax L.) in relation to water temperature and oxygenation. Aquacult. Res. 33, 607-613.
  • Cecchini S., Caputo A. R., 2003. Acid-base balance in sea bass (Dicentrarchus labrax L.) in relation to water oxygen concentration. Aquacult. Res. 34, 1069-1073.
  • Dabrowski K., Lee K. J., Guz L., Verlhac V., Gabaudan J., 2003. Effects of dietary ascorbic acid on oxygen stress (hypoxia or hyperoxia), growth and tissue vitamin concentrations in juvenile rainbow trout. Aquaculture 233, 383-392.
  • Farmer C. G., 1997. Did lungs and the intracardiac shunt evolve to oxygenate the heart in vertebrates? Paleobiology 23, 358-372.
  • Farrell A. P., Simonot D. L., Seymour R. S., Clark T. D., 2007. A novel techniques for estimating the compact myocardium in fishes reveals surprising results for an athletic air-breathing fish, the Pacific tarpon. J. Fish Biol. 71, 389-398.
  • Fievelstad S., Waagbo R., Stefansson S., Olsen A. B., 2007. Impacts of elevated water carbon dioxide partial pressure at two temperatures on Atlantic salmon (Salmo salar L.) parr growth and hematology. Aquaculture 269, 241-249.
  • Foss A., Evensen T. H., Øiestad V., 2002. Effects of hypoxia and hyperoxia on growth and food conversion efficiency in the spotted wolfish Anarhichas minor (Olafsen). Aquacult. Res. 33, 437-444.
  • Foss A., Vollen T., Øiestad V., 2003. Growth and oxygen consumption in normal and O2 supersaturated water, and interactive effects of O2 saturation and ammonia on growth in spotted wolfish (Anarhichas minor Olafsen). Aquaculture 224, 105-116.
  • Fraser J., Vieira de Mello L., Ward D., Rees H. H., Williams D. R., Fang Y., Brass A., Gracey A. Y., Cossins R., 2006. Hypoxia-inducible myoglobin expression in nonmuscle tissues. Proc. Natl. Acad. Sci. USA 103, 2977-2981.
  • Gałecka E., Jacewicz R., Mrowicka M., Florkowski A., Gałecki P., 2008. Enzymy antyoksydacyjne - budowa, właściwości, funkcje. Polski Merkuriusz Lekarski 25, 266-268.
  • Gnaiger E., Mendez G., Hand S. C., 2000. High phosphorylation efficiency and depression of uncoupled respiration in mitochondria under hypoxia. Proc. Natl. Acad. Sci. USA 97, 11080-11085.
  • Gonçalves A. F., Castro L. F. C., Pereira-Wilson C., Coimbra J., Wilson J. M., 2007. Is there a compromise between nutrient uptake and gas exchange in the gut of Misgurnus anguillicaudatus, an intestinal air-breathing fish? Comp. Biochem. Phys., Part D 2, 345-355.
  • Gonzalez R. J., Brauner C. J., Wang Y. X., Richards J. G., Patrick M. L., Xi W., Matey V., Val A.I., 2010. Impact of ontogenetic changes in branchial morphology on gill function in Arapaima gigas. Physiol. Biochem. Zool. 83, 322-332.
  • Good C., Davidson J., Welsh C., Snekvik K., Summerfelt S., 2010. The effect of carbon dioxide on performance and histopathology of rainbow trout Oncorhynchus mykiss in water recirculation aquaculture systems. Aquacult. Engin. 42, 51-56.
  • Graham J. B., 1997. Air-Breathing Fishes, Evolution, Diversity and Adaptation. Academic Press, San Diego, California.
  • Graham J. B, Lee H. J., 2004. Breathing air in air: in what ways might extant amphibious fish biology relate to prevailing concepts about early tetrapods, the evolution of vertebrate air breathing, and the vertebrate land transition? Physiol. Biochem. Zool. 77, 720-731.
  • Greenwood P. H., Liem K. E., 1984. Aspiratory respiration in Arapaima gigas (Teleostei, Osteoglossomorpha): A reappraisal. J. Zool. London 203, 411-425.
  • Hassell K. L., Coutin P. C., Nugegoda D., 2008. Hypoxia, low salinity and lowered temperature reduce embryo survival and hatch rates in black bream Acanthopagrus butcheri (Munro, 1949). J. Fish Biol. 72, 1623-1636.
  • Hill L. G., Renfro J. L., Reynolds R., 1972. Effects of dissolved oxygen tensions upon the rate of aerial respiration of young spotted gar, Lepisosteus oculatus (Lepisosteidae). South. Nat. 17, 273-278.
  • Hoogewijs D., Terwilliger N. B., Webster K. A., Powell-Coffman J. A., Tokishita S., Yamagata H., Hankeln T., Burmester T., Rytkönen K. T., Nikinmaa M., Abele D., Heise K., Lucassen M., Fandrey J., Maxwell P. H., Påhlman S., Gorr T. A., 2007. From critters to cancers: bridging comparative and clinical research on oxygen sensing, HIF signaling, and adaptation towards hypoxia. Integr. Comp. Biol. 47, 552-577.
  • Hosfeld C.D., Engevik A., Mollan T., Lunde T. M., Waagbø R., Olsen A. B., Breck O., Stefansson S., Fivelstad S., 2008. Long-term separate and combined effects of environmental hypercapnia and hyperoxia in Atlantic salmon (Salmo salar L.) smolts. Aquaculture 280, 146-153.
  • Hulbert W. C., Moon T. W., Hochachka P. W., 1978. The osteoglossid gill: correlations of structure, function, and metabolism with transition to air breating. Can. J. Zool. 56, 801-808.
  • Jaroszewska M., Dabrowski K., 2008. Morphological analysis of the functional design of the connection between alimentary tract and the gas bladder in air-breathing lepisosteid fish. Ann. Anat. 190, 383-390.
  • Jonz M. G., Nurse C. A., 2003. Neuroepithelial cells and associated innervation of the zabrafish gill: a confocal immunofluorescence study. J. Comp. Neurol. 461, 1-17.
  • Jonz M. G., Fearon I. M., Nurse C. A., 2004. Neuroepithelial oxygen chemoreceptors of the zebrafish gill. J. Physiol. 560, 737-752.
  • Jonz M. G, Nurse C. A., 2006. Ontogenesis of oxygen chemoreception in aquatic vertebrates. Respir. Physiol. Neurobiol. 154, 139-152.
  • Kajimura S., Aida K., Duan C., 2006. Understanding hypoxia-induced gene expression in early development: in vitro and in vivo analysis of hypoxia-inducible factor 1-regulated zebra fish insulin-like growth factor binding protein 1gene expression. Mol. Cell. Biol. 26, 1142-1155.
  • Kirschner M. W., Gerhart J. C., 2006. The plausibility of life. Yale University Press.
  • Korhea-Aho T. L., Partanen J. M., Kukkonen J. V. K., Taskinen J., 2008. Hypoxia increases intensity of epidermal papillomatosis in roach Rutilus rutilus. Dis. Aquat. Org. 78, 235-241.
  • Lechleuthner A., Schumacher U., Negele R. D., Welsh U., 1989. Lungs of Polypterus and Erpetoichthys. J. Morphol. 201, 161-178.
  • Lewis J. M., Costa I., Val A. L., Almeida-Val V. M. F., Gamperl A. K., Driedzic W. R., 2007. Responses to hypoxia and recovery: repayment of oxygen debt is not associated with compensatory protein synthesis in the Amazonian cichlid, Astronotus ocellatus. J. Exp. Biol. 210, 1935-1943.
  • Liem K. F., 1981. Larvae of air-breathing fishes as countercurrent flow devices in hypoxic environments. Science 211, 1177-1179
  • Liepelt A., Karbe L., Westendorf J., 1995. Induction of DNA strand breaks in rainbow trout Oncorhynchus mykiss under hypoxic and hyperoxic conditions. Aquatic Toxicol. 33, 177-181.
  • Lu G., Mak Y.T., Wai S.M., Kwong W.H., James A., Randall D., Yew D.T., 2005. Hypoxia-induced differential apoptosis in the central nervous system of the sturgeon (Acipenser shrenckii). MicroSC. Res. Tech. 68, 258-263.
  • Lushchak V., Bagnyukova T. V., 2006. Effects of different environmental oxygen levels on free radical processes in fish. Comp. Biochem. Physiol., Part B 144, 283-289.
  • MacCormack T. J., Treberq J. R., Almeida-Val V. M., Driedzic W.R., 2003. Mitochondrial KATP channels and sarcoplasmic reticulum influence cardiac force development under anoxia in the Amazonian armored catfish Liposarcus pardalis. Comp. Biochem. Physiol. 34, 441-448.
  • Mallat J., 1985. Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can. J. Fish. Aquatic Sci. 42, 630-648.
  • Morrison J. R., Deavours W. L., Jones J. C., Tabb M. A., 1995. Early rearing of channel catfish fry in floating raceways and subsequent survival in ponds. Prog. Fish-Culturist 57, 292-296.
  • Naňka O., Valášk P., Dvořáková M., Grim M., 2006. Experimental hypoxia and embryonic angiogenesis. Dev. Dynamics 235, 723-733.
  • Naňka O., Krizova P., Fikrle M., Tuma M., Blaha M., Grim M., Sedmera D., 2008. Abnormal myocardial and coronary vasculature development in experimental hypoxia. AnaT. Record 291, 1187-1199.
  • Neuenfeldt S., Andersen K. H., Hinrichsen H. H., 2009. Some Atlantic cod Gadus morhua in Baltic Sea visit hypoxic water briefly but often. J. Fish Biol. 75, 290-294.
  • Nikinmaa M., 2002. Oxygen-dependent cellular functions - why fishes and their aquatic environment are a prime choice of study. Comp. Biochem. Physiol., Part A 133, 1-16.
  • Nikinmaa M., Rees B. B., 2005. Oxygen-dependent gene expression in fishes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, 1079-1090.
  • Nilsson G. E., Östlund-Nilsson S., 2008. Does size matter for hypoxia tolerance in fish? Biol. Rev. 83, 173-189.
  • Olsvik P. A., Kristensen T., Waagbø R., Tollefsen K. E., Rosseland B. O., Toften H., 2006. Effects of hypo- and hyperoxia on transcription levels of five stress genes and the glutathione system in liver of Atlantic cod Gadus morhua. J. Exp. Biol. 209, 2893-2901
  • Ong K. J., Stevens E. D., Wright P. A., 2007. Gill morphology of the mangrove killifish (Kryptolebias marmoratus) is plastic and changes in response to terrestrial air exposure. J. Exp. Biol. 210, 1109-1115.
  • Ostaszewska T., Dabrowski K., Kamaszewski M., Grochowski P., Verri T., Rzepkowska M., Wolnicki J., 2010. The effect of plant protein-based diet supplemented with dipeptide or free amino acids on digestive tract morphology and PepT1 and PepT2 expressions in common carp (Cyprinus carpio L.). Comp. Biochem.Physiol. A, 157, 158-169.
  • Perry S. F., Wilson R. J. A., Straus C., Harris M. B., Remmers J. E., 2001. Which came first, the lung or the breath? Comp. Physiol. Biochem., Part A 129, 37-47.
  • Person-Le Ruyet J., Pichavant K., Vacher C., Le Bayon N., Sévère A., Boeuf G., 2002. Effects of O2 sueprsaturation on metabolism and growth in juvenile turbot (Scophthalamus maximus L.). Aquaculture 205, 373-383.
  • Pichavant K., Person-Le-Ruyet J., Le Bayon N., Sévère A., Le Roux A., Quéméner L., Maxime V., Nonnotte G., Boeuf G. 2000. Effects of hypoxia on growth and metabolism of juvenile turbot. Aquaculture 188, 103-114.
  • Plante S., Chabot D., Dutil J. D., 1998. Hypoxia tolerance in Atlantic cod. J. Fish Biol. 53, 1342-1356.
  • Podkowa D., Goniakowska-Witalińska L., 2003. Morphology of the air-breathing stomach of the catfish Hypostomus plecostomus. J. Morphol. 257, 147-163.
  • Pörtner H. O., Bock C., Knust R., Lanning G., Lucassen M., Mark F. C., Sartoris F. J., 2008. Cod and climate in a latitudinal cline: physiological analyses of climate effects in marine fishes. Climat Res. 37, 253-270.
  • Rahn H., Rahn K. B., Howell B. J., Gans C., Tenney S. M., 1971. Air breathing of the garfish (Lepisosteus osseus). RespiR. Physiol. 11, 285-307.
  • Renfro J. L., Hill L. G., 1970. Factors influencing the aerial breathing and metabolism of gars (Lepisosteus). Southwest. Nat. 15, 45-54.
  • Rinaldi L., Basso P., Tettamanti G., Grimaldi A., Terova G., Saroglia M., De Equileor M., 2005. Oxygen availability causes morphological changes and a different VEGF/Flk-1/HIF-2 expression in sea bass gills. Ital. J. Zool. 72, 103-111.
  • Robb T., Abrahams M.V., 2003. Variation in tolerance to hypoxia in a predator and prey species: an ecological advantage of being small? J. Fish Biol. 62, 1067-1081.
  • Roesner A., Hankel T., Burmester T., 2006. Hypoxia induces a complex response of globin expression in zebrafish (Danio rerio). J. Exp. Biol. 209, 2129-2137.
  • Saroglia M., Cecchini S., Terova G., Caputo A., De Stradis A., 2000. Influence of environmental temperature and water oxygen concentration on gas diffusion distance in sea bass (Dicentrarchus labrax, L.). Fish Physiol. Biochem. 23, 55-58.
  • Saroglia M., Terova G., De Stradis A., Caputo A., 2002. Morphometric adaptations of sea bass gills to different dissolved oxygen partial pressures. J. Fish Biol. 60, 1423-1430.
  • Satora L., 1998. Histological and ultrastructural study of the stomach of the air-breathing Ancistrus multispinnis (Siluriformes, Teleostei).Can. J. Zool. 76, 83-86.
  • Schmalhausen I. I., 1968. The origin of terrestrial vertebrates. Academic Press, New York.
  • Seymour R. S., Christian K., Bennett M. B., Baldwin J., Wells R. M. G., Baudinette R. V., 2004. Partitioning of respiration between the gills and air-breathing organ in response to aquatic hypoxia and exercise in the pacific tarpon, Megalops cyprinoides. Physiol. Biochem. Zool. 77, 760-767.
  • Smatresk N. J., Cameron J. N., 1982. Respiration and acid-base physiology of the spotted gar, a bimodal breather. I. Normal values, and the response to the severe hypoxia. J. Exp. Biol. 96, 263-280.
  • Smatresk N. J., Burleson M. L., Azizi S. Q., 1986. Chemoreflexive responses to hypoxia and NaCN in longnose gar: evidence for two chemoreceptors loci. Am. J. Physiol. 251, R116-R125.
  • Smatresk N. J., 1990. Chemoreceptor modulation of endogenous respiratory rhythms in vertebrates. Am. J. Physiol. 259, R887-R897.
  • Soitamo A. J., Rabergh C. M. J., Gassmann M., Sistonen L., Nikinmaa M., 2001. Characterization of a hypoxia-inducible factor (HIF-1α) from rainbow trout. J. Biol. Chem. 276, 19699-19705.
  • Sollid J., De Angelis P., Gundersen K., Nilsson G. E., 2003. Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J. Exp. Biol. 206, 3667-3673.
  • Sollid J., Kjernsli A., De Angelis P. M., Rohr A. K., Nilsson G. E., 2005. Cell proliferation and gill morphology in anoxic crucian carp. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, 1196-1201.
  • Sollid J., Rissanen E., Tranberg H. K., Thorstensen T., Vuori K. A. M., Nikinmaa M., Nilsson G. E., 2006. HIF-1α and iNOS levels in crucian carp gills during hypoxia-induced transormation. J. Comp. Physiol., Part B 176, 359-369.
  • Terova G., Rinoldi S., Cora S., Bernardini G., Gornati R., Saroglia M., 2008. Acute and chronic hypoxia affects HIF-1alfa mRNA levels in sea bass (Dicentrarchus labrax). Aquaculture 279, 150-159.
  • Val A. L. 1999. Water-air-breathing transition in fishes of the Amazon. [W:] Water/air transition in biology. Mittal A. K., Eddy F. B., Datta Munshi J. S. (red.). Oxford & IBN Publishing Co. PVT. LTD, 146-161.
  • Van der Meer D. L. M., Van den Thillart G. E. E. J. M., Witte F., de Bakker M. A. G., Besser J., Richardson M. K., Spaink H. P., Leito J. T. D., Bagowski C. P., 2005. Gene expression profiling of the long-term adaptive response to hypoxia in the gills of adult zebrafish. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R1512-R1519.
  • Van Raaij M. T. M., Bakker E., Nieveen M. C., Zirkzee H., van den Thillart G. E. E. J. M., 1994. Energy status and free fatty acid patterns in tissues of common carp (Cyprinus carpio, L.) and rainbow trout (Oncorhynchus mykiss, L.) during severe oxygen restriction. Comp. Biochem. Physiol. 109A, 755-767.
  • Villafañe V. E., Helbling W., Zagarese H. E., 2001. Solar ultraviolet radiation and its impact on aquatic systems of Patagonia, South America. Ambio 30, 112-117.
  • Vulesevic B., McNeill B., Perry S. F., 2006. Chemoreceptor plasticity and respiratory acclimation in the zebrafish Danio rerio. J. Exp. Biol. 209, 1261-1273.
  • Wells P.R., Pinder A. W., 2006. The respiratory development of Atlantic salmon II. Partioning of oxygen uptake among gills, yolk sac and body surfaces. J. Exp. Biol. 199, 2737-2744.
  • Wells R. M. G., Baldwin J., Seymour R. S., Christian K. A., Farrell A. P., 2007. Ar breathing minimizes post-exercise lactate load in the tropical Pacific tarpon, Megalops cyprinoides Broussonet 1782 but oxygen dept is required by aquatic breathing. J. Fish Biol. 71, 1649-1661.
  • Willson R. J. A., Harris M. B., Remmers J. E., Perry S. F., 2000. Evolution of air-breathing and central CO2/H+ respiratory chemosensitivity: new insights from an old fish? J. Exp. Biol. 203, 3505-3512.
  • Zaccone G., Fasulo S., Ainis L., Licata A., 1997. Paraneurons in the gills and airways of fishes. Micr. Res. Tech. 37, 4-12.
Document Type
Publication order reference
YADDA identifier
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.