title: Air breathing and aquatic gas exchange during hypoxia in armoured catfish.
abstract: Air breathing in fish is commonly believed to have arisen as an adaptation to aquatic hypoxia. The effectiveness of air breathing for tissue O2supply depends on the ability to avoid O2loss as oxygenated blood from the air-breathing organ passes through the gills. Here, we evaluated whether the armoured catfish (Hypostomus aff. pyreneusi)-a facultative air breather-can avoid branchial O2loss while air breathing in aquatic hypoxia, and we measured various other respiratory and metabolic traits important for O2supply and utilization. Fish were instrumented with opercular catheters to measure the O2tension (PO2) of expired water, and air breathing and aquatic respiration were measured during progressive stepwise hypoxia in the water. Armoured catfish exhibited relatively low rates of O2consumption and gill ventilation, and gill ventilation increased in hypoxia due primarily to increases in ventilatory stroke volume. Armoured catfish began air breathing at a water PO2of 2.5 kPa, and both air-breathing frequency and hypoxia tolerance (as reflected by PO2at loss of equilibrium, LOE) was greater in individuals with a larger body mass. Branchial O2loss, as reflected by higher PO2in expired than in inspired water, was observed in a minority (4/11) of individuals as water PO2approached that at LOE. Armoured catfish also exhibited a gill morphology characterized by short filaments bearing short fused lamellae, large interlamellar cell masses, low surface area, and a thick epithelium that increased water-to-blood diffusion distance. Armoured catfish had a relatively low blood-O2binding affinity when sampled in normoxia (P50of 3.1 kPa at pH 7.4), but were able to rapidly increase binding affinity during progressive hypoxia exposure (to a P50of 1.8 kPa). Armoured catfish also had low activities of several metabolic enzymes in white muscle, liver, and brain. Therefore, low rates of metabolism and gill ventilation, and a reduction in branchial gas-exchange capacity, may help minimize branchial O2loss in armoured catfish while air breathing in aquatic hypoxia.
authors.affiliation: Department of Biology, McMaster University, 1280 Main Street West, Hamilton, ON, L8S 4K1, Canada. scottg2@mcmaster.ca.
authors.forename: Graham R
authors.initials: GR
authors.lastname: Scott
authors.affiliation: Department of Biology, Center for Inland Waters, San Diego State University, San Diego, CA, 92182-4614, USA.
authors.forename: Victoria
authors.initials: V
authors.lastname: Matey
authors.affiliation: Department of Biology, McMaster University, 1280 Main Street West, Hamilton, ON, L8S 4K1, Canada.
authors.forename: Julie-Anne
authors.initials: JA
authors.lastname: Mendoza
authors.affiliation: Department of Biology, University of Ottawa, 30 Marie Curie Drive, Ottawa, ON, K1N 6N5, Canada.
authors.forename: Kathleen M
authors.initials: KM
authors.lastname: Gilmour
authors.affiliation: Department of Biology, University of Ottawa, 30 Marie Curie Drive, Ottawa, ON, K1N 6N5, Canada.
authors.forename: Steve F
authors.initials: SF
authors.lastname: Perry
authors.affiliation: Laboratory of Ecophysiology and Molecular Evolution, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Brazil.
authors.forename: Vera M F
authors.initials: VM
authors.lastname: Almeida-Val
authors.affiliation: Laboratory of Ecophysiology and Molecular Evolution, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Brazil.
authors.forename: Adalberto L
authors.initials: AL
authors.lastname: Val
mesh_terms: D000388:Air; D000818:Animals; D001921:Brain / Q000378:metabolism; D002397:Catfishes / Q000033:anatomy & histology / Q000378:metabolism* / Q000502:physiology*; D002950:Citrate (si)-Synthase / Q000378:metabolism; D003576:Electron Transport Complex IV / Q000378:metabolism; D029941:Fish Proteins / Q000378:metabolism; D005880:Gills / Q000033:anatomy & histology / Q000502:physiology* / Q000648:ultrastructure; D000860:Hypoxia / Q000378:metabolism* / Q000503:physiopathology*; D007770:L-Lactate Dehydrogenase / Q000378:metabolism; D008099:Liver / Q000378:metabolism; D008855:Microscopy, Electron, Scanning; D018482:Muscle, Skeletal / Q000378:metabolism; D009211:Myoglobin / Q000378:metabolism; D010101:Oxygen Consumption; D019764:Phosphoenolpyruvate Carboxykinase (ATP) / Q000378:metabolism; D011770:Pyruvate Kinase / Q000378:metabolism; D012119:Respiration
chemical_list: D029941:Fish Proteins; D009211:Myoglobin; D007770:L-Lactate Dehydrogenase; D003576:Electron Transport Complex IV; D002950:Citrate (si)-Synthase; D011770:Pyruvate Kinase; D019764:Phosphoenolpyruvate Carboxykinase (ATP)
keywords: Calophysus macropterus; Gas exchange; Gill; Haemoglobin; Myoglobin; Teleost; Ventilation