The gill is the main respiratory organ in most fishes; however, some species obtain O2 directly from atmospheric air by using modified structures in the head or digestive tract (Graham, 1997). The gills of all fishes are similar in their basic structure. Morphometric differences are usually related to the number and size of gill elements (filament and lamella) that affect the efficiency of O2 uptake and are associated with the oxygen needs and/or their habitats (Gray, 1954; Hughes, 1984; Fernandes, 1996; Fernandes et al., 2007; Duncan and Fernandes, 2010). Active and/or hypoxia-tolerant fishes are characterized by a large number of long filaments, a great number of lamellae per millimeter of filament length and, consequently, a large respiratory surface area (Santos et al., 1994; Fernandes, 1996; Mazon et al., 1998; Fernandes et al., 2007; Chapman, 2007). 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).
In air-breathing fish, the gills exhibit irreversible changes in morphology depending on the relative dependence on water or air for gas exchange (Low et al., 1988; Mattias et al., 1996, 1998; Perna and Fernandes, 1996; Takasusuki et al., 1998; Wilson et al., 1999; Graham et al., 2007). The smallest gill surface area has been documented for the South American lungfish, Lepidosiren paradoxa (Lepidosirenidae), which has irregularly arranged short papillar gill lamellae. These gills are unable to take up the necessary amount of O2 to support oxidative metabolism (Wright, 1974; Moraes et al., 2005) which is provided by the well-developed lungs, evolved during exposure to chronic hypoxia along evolutionary time scale (Johansen and Lenfant, 1967; Bassi et al., 2005; Moraes et al., 2005). Among the Teleostei, the development of a swim bladder modified for O2 uptake from atmospheric air in the pirarucu, Arapaima gigas, allowed changes in the gill morphology as fish developed. Fish is exclusively water-breathing until nine days post-hatch (∼1 g, 1.8 cm length) (Lüling, 1964) and, during development, the fish become dependent on atmospheric air (Sawaya, 1946; Graham, 1997). These fish are then known as obligate air-breathing fish. A. gigas is endemic to the Amazon Basin and is one of largest freshwater fish: it grows up to 4,000–5,000 g (∼80 cm length) in its first year of life (Val and Almeida-Val, 1995) and reaches up to 250,000 g (2–3 m length) over the course of its lifespan (Saint-Paul, 1986; Salvo-Souza and Val, 1990). Without access to air, a 10 g (∼12 cm; 1 month old) fish can survive twice as long as a 1,000 g (∼50 cm; 5–7 months old) fish can (Brauner et al., 2004). In fish lower than 1,000 g the gills are responsible for 23–30% of the whole-body O2 uptake (Gonzales et al 2010) but, in fish between 1,000 and 2,000 g fish, only 20–25% of O2 are took up by the gills (Sawaya, 1946; Stevens and Holeton, 1978; Brauner and Val, 1996). Conversely, CO2 is primarily excreted by the gills (63–78%) and, to a lesser extent, by the swim bladder (15%) and kidney (6%) (Hulbert et al., 1978; Stevens and Holeton, 1978; Brauner and Val, 1996). At low magnification, scanning electron microscopy (SEM) revealed well-developed lamellae in the gill filaments of 10–100 g fish (∼22–25 cm; 2–3 months old) but not in those of 724 g and 1,000 g fish (Brauner et al., 2004; Gonzalez et al., 2010). The lamellar organization of a 100 g A. gigas is similar to that of other teleosts, and its respiratory surface area is similar to those of facultative air-breathing fish of a similar size (Costa et al., 2007); the average respiratory surface area of the swim bladder exceeded that of the gills by a factor of 2.8 indicating the importance of the swim bladder for respiration, even in juvenile fish (Fernandes et al., 2012). Data concerning ion regulation has demonstrated that the rate of diffusive Na+ loss is higher in 724 g fish (∼45 cm; 5 months old) than in 67 g fish (∼22 cm, 2 months old) (Gonzalez et al., 2010) and Brauner et al. (2004) identified high density of mitochondria-rich cells (MRCs) along the outer cell layer of the filament epithelium of 1,000 g fish. However, the changes in the lamellar structure and the morphological processes involved in the gill remodeling of A. gigas during development are not yet known.