The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii

Abstract

SUMMARYGoldfish and crucian carp at low temperature exhibit plasticity in gill morphology during exposure to hypoxia to enhance gas exchange. Hypoxia-induced changes in gill morphology and cellular ultrastructure of the high altitude scaleless carp from Lake Qinghai, China, were investigated to determine whether this is a general characteristic of cold water carp species. Fish were exposed to acute hypoxia (0.3·mg·O 2 ·l -1 ) for 24·h followed by 12·h recovery in normoxic water (6·mg·O 2 ·l -1 at 3200·m altitude), with no mortality. Dramatic alterations in gill structure were initiated within 8·h of hypoxia and almost complete by 24·h, and included a gradual reduction of filament epithelial thickness (>50%), elongation of respiratory lamellae, expansion of lamellar respiratory surface area (>60%) and reduction in epithelial water-blood diffusion distance (<50%). An increase in caspase 3 activity in gills occurred following 24·h exposure to hypoxia, indicating possible involvement of apoptosis in gill remodeling. Extensive gill mucous production during hypoxia may have been part of a general stress response or may have played a role in ion exchange and water balance. The large increase in lamellar surface area and reduction in diffusion distance presumably enhances gas transfer during hypoxia (especially in the presence of increased mucous production) but comes with an ionoregulatory cost, as indicated by a 10 and 15% reduction in plasma [Na

Warm acclimation improves hypoxia tolerance in Fundulus heteroclitus

“…Remodelling of gill morphology has primarily been investigated in the context of acclimation to hypoxia (e.g. Crispo and Chapman, 2010), and this has been shown to occur via changes in the ILCM in a variety of fish species (Sollid et al, 2003(Sollid et al, , 2005aNilsson, 2007;Ong et al, 2007;Matey et al, 2008;Turko et al, 2012;Dhillon et al, 2013;Johannsson et al, 2014;Anttila et al, 2015) including killifish (Borowiec et al, 2015). Less is known about the effects of thermal acclimation on gill morphology, but decreases in the ILCM at warmer temperatures have been observed in crucian carp, goldfish (Sollid et al, 2005b;Mitrovic and Perry, 2009) and killifish (Barnes et al, 2014).…”

“…Because this approximation does not take into account the potential for gas exchange along the 'top' of the lamella, it may underestimate lamellar surface area; however, analysis of previously published data (e.g. Matey et al, 2008;Brauner et al, 2011) suggests that it results in no more than a 10% reduction in estimated area compared with an approach modelling the lamellae as a half-ellipsoid (e.g. Matey et al, 2008), and it does not change the relationship among groups.…”

“…Matey et al, 2008;Brauner et al, 2011) suggests that it results in no more than a 10% reduction in estimated area compared with an approach modelling the lamellae as a half-ellipsoid (e.g. Matey et al, 2008), and it does not change the relationship among groups.…”

A unique mode of tissue oxygenation and the adaptive radiation of teleost fishes

“…In addition, changes in blood flow through each lamella may enhance gill diffusing capacity (for details, see Randall and Daxboeck, 1984). Another means for increasing diffusing capacity during hypoxia (but not anoxia) has been observed in carp, where an interlamellar epithelial cell mass between the gill lamellae is removed through apoptosis (Sollid et al, 2003), which increases gill surface area and decreases epithelium diffusion distance (Matey et al, 2008). Fish increase blood Hb concentrations during hypoxia but, unlike mammals, many teleost fishes also increase Hb-oxygen (Hb-O 2 ) affinity (Val, 2000) by decreasing levels of organic phosphates (e.g.…”

Prolonged apoptosis in mitochondria-rich cells of tilapia (Oreochromis mossambicus) exposed to elevated salinity

“…This physiological mechanism is important during development, diVerentiation of tissues and organ systems, and for removing terminally damaged cells (Yamashita et al 2008;Matey et al 2008;Kültz 2005). Measurements of apoptosis in teleost gill cells in response to salinity stress are sparse.…”