Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills

Abstract

SUMMARYWe show that crucian carp (Carassius carassius) living in normoxic(aerated) water have gills that lack protruding lamellae, the primary site of O2 uptake in fish. Such an unusual trait leads to a very small respiratory surface area. Histological examination showed that the lamellae(secondary lamellae) of these fish were embedded in a cell mass (denoted embedded lamellae). When the fish were kept in hypoxic water, a large reduction in this cell mass occurred, making the lamellae protrude and increasing the respiratory surface area by ∼7.5-fold. This morphological change was found to be reversible and was caused by increased apoptosis combined with reduced cell proliferation. Carp with protruding lamellae had a higher capacity for oxygen uptake at low oxygen levels than fish with embedded lamellae, but water and ion fluxes appeared to be increased, which indicates increased osmoregulatory costs. This is, to our knowledge, the first demonstration of an adaptive and reversible gross morphological change in the respiratory organ of an adult vertebrate in response to changes in the availability of oxygen.

Improving aeration for efficient oxygenation in sea bass sea cages. Blood, brain and gill histology

“…Changes in environmental variables, such as the water oxygen content and temperature, can also cause fish to dramatically change the morphology of their gills in a rapid and reversible manner. Reports in the literature indicate that several species (Oncorhynchus mykiss, Rutilus rutilus, Perca fluviatilis, Anguilla anguilla, Ambloplites rupestris, Micropterus salmoides, and Carassius carassius) can reduce their respiratory surface area, to some extent, when challenged with unfavourable conditions (soft water, low pH or metals) and/or when exposed to low temperatures, which would reduce the oxygen demand [24,[47][48][49][50][51]. The goldfish is extremely hypoxia-tolerant and has haemoglobin with a very high oxygen affinity [52].…”

“…There could be gill morphological changes occurring after exposure to hypoxic conditions. According to Sollid et al [24] these changes are a combination of reduced cell proliferation and an induction of apoptosis. The brain is about 2% of the total body mass and accounts for 20% of total oxygen consumption.…”

Identification and characterization of hypoxia-induced genes in Carassius auratus blastulae embryonic cells using suppression subtractive hybridization

“…Since water has a low oxygen capacity and poor oxygen diffusibility, many fish species have evolved behavioral, anatomical, physiological, biochemical and molecular adaptations that enable them to cope with periods of hypoxia (Wu, 2002;Nikinmaa, 2002;Nilsson and Ostlund-Nilsson, 2004). Hypoxia has been revealed to cause significant morphological and gene transcription changes in fish (Gracey et al, 2001;Ton et al, 2003;Sollid et al, 2003Sollid et al, , 2005David et al, 2005). However, the molecular mechanisms of hypoxia tolerance in fish remain largely unknown.…”

“…Both in nature and in the laboratory, they have been found to survive many days or, at low temperatures, even several months of anoxia Piironen and Holopainen, 1986;Nilsson and Lutz, 2004). Some of the adaptive mechanisms the Carassius species have evolved to survive anoxia include the ability of producing ethanol as an alternative metabolic end product (Shoubridge and Hochachka, 1980;Johnston and Bernard, 1983), increasing respiratory surface area to boost oxygen uptake (Sollid et al, 2003(Sollid et al, , 2005, maintaining heart activity and brain ATP levels for several days (Nilsson, 2001;Stecyk et al, 2004). These striking differences in anoxic survival strategy are reflected all the way down to the cellular and molecular levels.…”

Implications for Osmorespiratory Compromise by Anatomical Remodeling in the Gills of Arapaima gigas

“…Conversely, the gills of sluggish or benthic fishes have low numbers of lamellae per millimeter of filament length and thus display a small respiratory surface area (Gray, 1954;Hughes, 1984). Recently, the plasticity of the gill dimensions and the reversible remodeling of gill morphology have been studied in fish exposed to pollutants and transferred to clean water (Cerqueira and Fernandes, 2002;Fernandes and Mazon, 2003;Nilsson et al, in press), in response to hypoxia and temperature (Sollid et al, 2003;Sollid and Nilsson, 2006;Perry et al, 2012) and during defense against parasite infections (Nilsson et al, 2012).…”