title: The transition from water-breathing to air-breathing is associated with a shift in ion uptake from gills to gut: a study of two closely related erythrinid teleosts, Hoplerythrinus unitaeniatus and Hoplias malabaricus.
abstract: The evolutionary transition from water-breathing to air-breathing involved not only a change in function of the organs of respiratory gas exchange and N-waste excretion, but also in the organs of ion uptake from the environment. A combination of in vivo and in vitro techniques was used to look at the relative importance of the gills versus the gut in Na(+), Cl(-), and K(+) balance in two closely related erythrinid species: a facultative air-breather, the jeju (Hoplerythrinus unitaeniatus) and an obligate water-breather, the traira (Hoplias malabaricus). The jeju has a well-vascularized physostomous swimbladder, while that in the traira is poorly vascularized, but the gills are much larger. Both species are native to the Amazon and are common in the ion-poor, acidic blackwaters of the Rio Negro. Under fasting conditions, the traira was able to maintain positive net Na(+) and Cl(-) balance in this water, and only slightly negative net K(+) balance. However, the jeju was in negative net balance for all three ions and had lower plasma Na(+) and Cl(-) concentrations, despite exhibiting higher branchial Na(+), K(+)ATPase and v-type H(+)ATPase activities. In the intestine, activities of these same enzymes were also higher in the jeju, and in vitro measurements of net area-specific rates of Na(+), Cl(-), and K(+) absorption, as well as the overall intestinal absorption capacities for these three ions, were far greater than in the traira. When acutely exposed to disturbances in water O2 levels (severe hypoxia ~15% or hyperoxia ~420% saturation), gill ionoregulation was greatly perturbed in the traira but less affected in the jeju, which could "escape" the stressor by voluntarily air-breathing. We suggest that a shift of ionoregulatory capacity from the gills to the gut may have occurred in the evolutionary transition to air-breathing in jeju, and in consequence branchial ionoregulation, while less powerful, is also less impacted by variations in water O2 levels.
authors: Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada. woodcm@mcmaster.ca.|Department of Biology, McMaster University, Hamilton, ON, Canada. woodcm@mcmaster.ca.|Rosenstiel School of Marine and Atmospheric Science, University of Miami, Coral Gables, FL, USA. woodcm@mcmaster.ca.|Laboratory of Ecophysiology and Molecular Evolution, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Amazonas, Brazil. woodcm@mcmaster.ca.
authors: Chris M
authors: CM
authors: Wood
authors: Laboratory of Ecophysiology and Molecular Evolution, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Amazonas, Brazil.|Institute of Zoology, University of Innsbruck, Innsbruck, Austria.|Center for Molecular Biosciences, University of Innsbruck, Innsbruck, Austria.
authors: Bernd
authors: B
authors: Pelster
authors: Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada.|Laboratory of Ecophysiology and Molecular Evolution, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Amazonas, Brazil.
authors: Marina
authors: M
authors: Giacomin
authors: Laboratory of Ecophysiology and Molecular Evolution, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Amazonas, Brazil.
authors: Helen
authors: H
authors: Sadauskas-Henrique
authors: Laboratory of Ecophysiology and Molecular Evolution, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Amazonas, Brazil.
authors: Vera Maria F
authors: VM
authors: Almeida-Val
authors: Laboratory of Ecophysiology and Molecular Evolution, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Amazonas, Brazil.
authors: Adalberto Luis
authors: AL
authors: Val
mesh_terms: D000388:Air; D000818:Animals; D060125:Characiformes / Q000502:physiology*; D002712:Chlorides / Q000097:blood / Q000378:metabolism; D005880:Gills / Q000378:metabolism / Q000502:physiology*; D000860:Hypoxia; D007408:Intestinal Absorption; D007413:Intestinal Mucosa / Q000378:metabolism; D007422:Intestines / Q000502:physiology*; D007477:Ions / Q000378:metabolism*; D011188:Potassium / Q000378:metabolism; D012143:Respiratory Physiological Phenomena; D012964:Sodium / Q000097:blood / Q000378:metabolism; D000254:Sodium-Potassium-Exchanging ATPase / Q000378:metabolism; D013045:Species Specificity
chemical_list: D002712:Chlorides; D007477:Ions; D012964:Sodium; D000254:Sodium-Potassium-Exchanging ATPase; D011188:Potassium
keywords: Gut sacs; Hyperoxia; Hypoxia; Jeju; Na+,K+ATPase; Swimbladder; Traira; v-type H+ATPase