A Fish Out of Water: Gill and Skin Remodeling Promotes Osmo- and Ionoregulation in the Mangrove KillifishKryptolebias marmoratus

Abstract

The euryhaline, amphibious mangrove killifish Kryptolebias marmoratus is known to survive weeks out of water in moist environments. We tested the hypothesis that the skin is a site of osmo- and ionoregulation in K. marmoratus. We predicted that under terrestrial conditions, gill and skin remodeling would result in an enhanced role for skin and a diminished role for the gills in osmo- and ionoregulation. Fish were exposed to water-either freshwater (FW, 1‰) or hypersaline water (saltwater [SW], 45‰)-or air over a moist surface of FW or SW for 9 d and then recovered in water. When fish were emersed for 9 d, (22)Na and (3)H-H(2)O were exchanged across the cutaneous surface. Homeostasis of whole-body Cl(-) and water levels but not of Na(+) levels was maintained over 9 d in air. In air-exposed fish, there was a significant increase in the size of skin ionocytes (in SW), a decrease in the number of skin mucous cells (in SW), and an increase in the gill interlamellar cell mass relative to those of fish in water. Gill ionocytes were mostly embedded away from the external surface in air-exposed fish, but the number and size of ionocytes increased (in FW). Interestingly, skin ionocytes formed distinct clusters of 20-30 cells. The estimated number of ionocytes over the whole skin surface was comparable to that in the gills. Overall, the findings support the hypothesis that the skin is a site of osmo- and ionoregulation in K. marmoratus in aquatic and terrestrial environments. Reversible cellular and morphological changes to the skin and gills during air exposure probably enhanced the cutaneous contribution to ion and water balance.

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

“…We observed significant increases in the ILCMs of fish exposed to air or low ion water, as has been previously observed (Ong et al, 2007;LeBlanc et al, 2010). We also found that 7days of hypoxic acclimation significantly decreased the height of the ILCM in mangrove rivulus.…”

“…While this is the first report of hypoxia-induced gill plasticity in K. marmoratus, this response was not surprising based on previous studies in hypoxia-acclimated cyprinid fishes, where an increase in gill surface area would likely facilitate oxygen uptake (Sollid et al, 2003;Matey et al, 2008;Mitrovic et al, 2009). Enlarged ILCMs during acclimation to low ion water is thought to reduce ion loss at the expense of reduced respiratory function according to the osmorespiratory compromise hypothesis (Gonzalez and McDonald, 1992;LeBlanc et al, 2010).…”

“…Functional gill surface area is inversely related to the height of the ILCM, as the ILCM occupies the space between adjacent lamellae and determines the proportion of each lamella exposed to the environment. The ILCMs adjacent to five randomly selected lamellae from each gill arch were measured, and the 20 measurements were averaged to provide a mean value for each individual (LeBlanc et al, 2010).…”

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

“…The kidney is one organ that became more important in ionoregulation (Smith 1959;Brauner et al 2004), but the kidney can only retain and regulate ions, not acquire them from the environment, which is a critical requirement for freshwater fish. There is also evidence that the skin became an important site of ion uptake, at least transitionally (Wilkie et al 2007;LeBlanc et al 2010), but in the longer term, it seems that this function must have been taken over by the gut once contact with water was lost during the evolutionary transition to life on land.…”

Amphibious fishes: evolution and phenotypic plasticity

“…Yokota et al, 1997;LeBlanc et al, 2010;Itoki et al, 2012;Cooper et al, 2013). In K. marmoratus acclimated to air on a hypersaline surface, skin ionocyte cross-sectional area increased, although ionoregulation was not perfectly maintained, as whole-body Na + levels were 30% higher relative to those of control fish in water .…”