Gill remodelling during terrestrial acclimation reduces aquatic respiratory function of the amphibious fishKryptolebias marmoratus

Abstract

SUMMARYThe skin-breathing amphibious fish Kryptolebias marmoratus experiences rapid environmental changes when moving between water-and air-breathing, but remodelling of respiratory morphology is slower (~1week). We tested the hypotheses that (1) there is a trade-off in respiratory function of gills displaying aquatic versus terrestrial morphologies and (2) rapidly increased gill ventilation is a mechanism to compensate for reduced aquatic respiratory function. Gill surface area, which varied inversely to the height of the interlamellar cell mass, was increased by acclimating fish for 1week to air or low ion water, or decreased by acclimating fish for 1week to hypoxia (~20% dissolved oxygen saturation). Fish were subsequently challenged with acute hypoxia, and gill ventilation or oxygen uptake was measured. Fish with reduced gill surface area increased ventilation at higher dissolved oxygen levels, showed an increased critical partial pressure of oxygen and suffered impaired recovery compared with brackish water control fish. These results indicate that hyperventilation, a rapid compensatory mechanism, was only able to maintain oxygen uptake during moderate hypoxia in fish that had remodelled their gills for land. Thus, fish moving between aquatic and terrestrial habitats may benefit from cutaneously breathing oxygen-rich air, but upon return to water must compensate for a less efficient branchial morphology (mild hypoxia) or suffer impaired respiratory function (severe hypoxia). Supplementary material available online at

The hypoxia signaling pathway and hypoxic adaptation in fishes

“…Second, they alter the shape and structure of the gill to enhance oxygen exchange [41][42][43][44][45][46]. Some fishes alter the cardiac K(ATP) channel, metabolic rate, and increase the number of red blood cells [47,48].…”

“…The Indian catfish is a hypoxia-tolerant species, in which short-term exposure to hypoxia induces HIF-1α and HIF-2α expression in the brain, liver, and kidney, whereas the long-term exposure induces HIF-1α expression in the spleen and HIF-2α expression in muscle [57]. Furthermore, in channel catfish, another hypoxia-tolerant fish, HIF-α mRNA expression decreases under hypoxia for the first 1.5 h and then increases after 5 h [42].…”

The amphibious fishKryptolebias marmoratususes alternate strategies to maintain oxygen delivery during aquatic hypoxia and air exposure

“…Instead of recruiting additional sites of gas exchange to tolerate hypoxia, mangrove rivulus appear to increase their capacity for branchial O 2 uptake by increasing gill surface area by reduction of the inter-lamellar cell mass (Turko et al, 2012). During emersion, amphibious fishes often rely on air-breathing organs such as lungs, buccal pouches or capillary-rich cutaneous surfaces (Johansen, 1970;Satchell, 1976;Olson, 1994;Graham, 1997).…”

“…Augmented cutaneous blood flow increases O 2 uptake and probably allowed mangrove rivulus to reduce evaporative water loss by decreasing aerial ventilation frequency (Burggren and Mwalukoma, 1983; Burggren and Moalli, 1984). Air exposure also induces enlargement of the inter-lamellar cell mass, reducing the effective gill surface area, which may further limit water loss during bucco-opercular ventilation (Ong et al, 2007).Observing bucco-opercular respiration was highly unexpected, considering gill surface area is reduced during air exposure and the branchial region was presumed to be non-functional (Ong et al, 2007;Cooper et al, 2012). Instead, aerial O 2 uptake in this species was thought to be achieved entirely across the cutaneous epithelium (Wright, 2012).…”

“…In the wild, mangrove rivulus typically inhabit extremely hypoxic (P O 2 <2.5kPa) puddles and crab burrows filled with water, but these fish also frequently emerse and find refuge in terrestrial habitats such as damp leaf litter or inside rotting logs that may also be hypoxic (Taylor et al, 2008, Ellison et al, 2012Taylor, 2012). Emersions can last upwards of 2 months (Taylor, 1990), during which time mangrove rivulus remain active and are thought to obtain O 2 by cutaneous respiration (Grizzle and Thiyagarajah, 1987;Cooper et al, 2012;Wright, 2012). To test the hypothesis that air-exposed fish mount a hypoxia response, we exposed K. marmoratus to 7 days of aquatic normoxia, aquatic hypoxia (P O 2 ~3.6kPa), aerial normoxia or aerial hypoxia (P O 2 ~13.6 kPa).…”