Oxygen consumption and hematological and biochemical parameters changes of the snakehead, Channa argus during aerial respiration

This study aimed to test the hypothesis that the aerial survival of the northern snakehead is involved not only with suprabranchial chamber respiration but also with physiological regulations. The aerial survival time and oxygen consumption rate (VO2) were determined in snakeheads with either normal or injured suprabranchial organs. Some hematological and biochemical parameters were assessed during aerial exposure. The results showed that resting VO2 decreased when switching from water to air in both the control and the suprabranchial organ-injured fish, with decreases of 22.4 and 23.5%, respectively. Resting VO2 in air was not different between the control and the suprabranchial organ-injured fish. The red blood cell (RBC) count and hemoglobin concentration showed no marked changes, while RBC size increased when exposed to air. The liver lactate concentration remained unchanged, and the white muscle lactate concentration decreased when switching from water to air. The blood ammonia concentration tended to increase during aerial respiration. The results suggest that the aerial survival of the snakehead is positively associated with a combination of factors, including respiration of suprabranchial organs and other accessory organs, depressed metabolic demands, and increased oxygen transport, and negatively associated with the accumulation of blood ammonia but not anaerobic metabolism. B io lo gy O pe n • A cc ep te d m an us cr ip t by guest on January 27, 2018 http://bio.biologists.org/ Downloaded from Introduction The northern snakehead (Channa argus) is a species of air-breathing fish that is widely distributed in East Asia. This fish has a peculiar accessory breathing organ, the suprabranchial chamber, by which the fish breathes air at the water’s surface using a cough-like mechanism (Ishimatsu and Itazawa, 1981; Lefevre et al., 2014), making possible short-term survival out of water (Nagata and Nakata, 1988). The suprabranchial chamber of Channa possesses a richly vascularized wall for gas exchange. It communicates with the buccopharyngeal cavity through a ventral opening guarded by a ‘shutter’ plate bone outgrowth of the first branchial arch, which can close the inhalant aperture of the suprabranchial chamber during expiration (Munshi, 1962). Even though many air-breathing fish maintain equivalent oxygen consumption in air and in water (Yoshiyama and Cech, 1994; Sayer, 2005), some air-breathing fishes reduce their oxygen consumption rate (VO2) in air (Garey, 1962; Martin et al., 2004; Lefevre et al., 2014). Our recent study has found that the northern snakehead can depress metabolic level in air (Li et al., 2017), implying that the snakehead may have mechanisms other than its suprabranchial chamber to meet metabolic demands and survive out of water. In addition to ventilation, some other physiological regulations may be necessary for fish to breathe air (Sayer, 2005). Fish may improve their blood oxygen-carrying capacity to compensate for their impaired oxygen uptake and/or enhance anaerobic metabolism (which is indicated by lactic acid concentration) during aerial exposure (Farmer, 1979; Bennett, 1978; Martin, 1995; Graham, 1997). Whether these regulations occur in the northern snakehead during aerial exposure to compensate for air respiration of the suprabranchial organ remains unclear. Short-term aerial survival has been reported in several Channa species, e.g., 8 h for C. striata, more than 27 h for C. batrachus (Chandra, 2001; Chandra and Banerjee, 2004), and 14 to 24 h for the northern snakehead depending on ambient temperature and metabolic demand (Li et al., 2017). It has been suggested that air respiration of the snakehead via the cough-like ventilation mechanism is water dependent (Ishimatsu and Itazawa, 1981) and therefore that the snakehead would be unable to survive in terrestrial habitats for very long (Liem, 1984). An alternative mechanism for the aerial survival of fish could be ammonia poisoning. In water, the ammonia products of fish are excreted easily and diffuse rapidly (Mommsen and Walsh, 1992; Wood, 1993). Out of water, however, the ammonia excretion of the fish may be blocked, which may lead to an accumulation of ammonia in the fish body B io lo gy O pe n • A cc ep te d m an us cr ip t by guest on January 27, 2018 http://bio.biologists.org/ Downloaded from (Chew, 2003; Sayer, 2005). Therefore, it can be hypothesized that the limited aerial survival of the northern snakehead could be attributed to excess ammonia accumulation. We assumed that the aerial survival of the snakehead is involved not only with suprabranchial chamber respiration but also with physiological regulations, such as depressed metabolic demands, enhanced blood oxygen-carrying capacity, and enhanced anaerobic metabolism. The oxygen consumption of fish with normal or injured suprabranchial chambers was compared to test the contribution of the suprabranchial chamber to oxygen uptake. VO2, blood parameters, lactate content of liver and muscle, and plasma ammonia were also assessed to test the changes in oxygen-carrying capacity, anaerobic metabolism, and ammonia accumulation of the fish when switched from water-breathing to air-breathing.