Metabolic adjustments in two Amazonian cichlids exposed to hypoxia and anoxia

Abstract

The effects of graded hypoxia on the physiological and biochemical responses were examined in two closely related species of cichlids of the Amazon: Astronotus crassipinnis and Symphysodon aequifasciatus. Ten fish of each species were exposed to graded hypoxia for 8 h in seven oxygen concentrations (5.92, 3.15, 1.54, 0.79, 0.60, 0.34, and 0.06 mg O(2) L(-)(1)), with the aim to evaluate hypoxia tolerance and metabolic adjustments, where plasma glucose and lactate levels, hepatic and muscle glycogen contents, and maximum enzyme activities (PK, LDH, MDH and CS) in skeletal and cardiac muscles were measured. Another experimental set was done to quantify oxygen consumption (MO(2)) and opercular movements in two oxygen concentrations. Hypoxia tolerance differed between the two species. Astronotus crassipinnis was able to tolerate anoxia for 178 min while S. aequifasciatus was able to withstand 222 min exposure in deep hypoxia (0.75 mg O(2) L(-)(1)). Suppressed MO(2) was observed during exposure to 0.34 (A. crassipinnis) and 0.79 mg O(2) L(-)(1) (S. aequifasciatus), while opercular movements increased in both species exposed to hypoxia. Higher levels of muscle and liver glycogen and larger hypoxia-induced increases in plasma glucose and lactate were observed in A. crassipinnis, which showed a higher degree of hypoxia tolerance. Changes in enzyme levels were tissue-specific and differed between species suggesting differential abilities in down-regulating oxidative pathways and increasing anaerobic metabolism. Based on the present data, we conclude that these animals are good anaerobes and highly adapted to their environment, which is allowed by their abilities to regulate metabolic pathways and adjust their enzyme levels.

Interactions between hypoxia tolerance and food deprivation in Amazonian oscars, Astronotus ocellatus (Agassiz)

“…Very few changes occurred in energy stores under the few hours of severe hypoxia, except for a decrease in total liver lipid and total energy content. Earlier studies on A. ocellatus and Astronotus crassipinnis exposed to hypoxia levels between 7 and 15 Torr for 8-20 h showed a depressed energy metabolism with increased plasma glucose and lactate and muscle lactate levels, but without many changes in tissue energy stores (Chippari-Gomes et al, 2005;Richards et al, 2007). In A. crassipinnis, liver glycogen dropped after 3 h of hypoxia at 7 Torr, but not at 15 Torr (Chippari-Gomes et al, 2005), and in A. ocellatus liver glycogen levels returned to control levels after 20 h, following an initial increase at 7 Torr (Richards et al, 2007).…”

“…Studies on several fish species, including oscars, have identified multiple adaptive strategies to survive hypoxia and even anoxia (Almeida-Val and Hochachka, 1995;Muusze et al, 1998). Strategies involve substantial metabolic depression and increased use of anaerobic metabolic pathways (Muusze et al, 1998;Almeida-Val et al, 2000;Chippari-Gomes et al, 2005) rather than increased oxygen extraction efficiency (Scott et al, 2008), traits that scale positively with fish size (Almeida-Val et al, 2000;Sloman et al, 2006). Ventilation does increase under hypoxia (Chippari-Gomes et al, 2005; Scott et al, 2008), which puts the fish at risk of losing more ions to their extremely dilute environment due to the osmo-respiratory compromise (Randall et al, 1972;Nilsson, 2007).…”

Physiological tradeoffs may underlie the evolution of hypoxia tolerance and exercise performance in sunfish (Centrarchidae)

“…Scott et al, 2008), so the spongy myocardium may require the use of anaerobic metabolism to maintain ATP supply. Consistent with this possibility, hypoxia acclimation increases the activity of glycolytic and anaerobic enzymes in the heart of some hypoxiatolerant species (Chippari-Gomes et al, 2005;Martínez et al, 2006). The increase in LDH activity in particular may also increase the capacity of the heart to oxidize the lactate produced by other tissues in hypoxia.…”

Origins of variation in muscle cytochrome c oxidase activity within and between fish species

“…Photoperiod can induce modifications in mitochondria in both Atlantic cod (Pelletier et al, 1993) and rainbow trout (Martin et al, 2009). Oxygen is well known to affect the glycolytic phenotype (Chippari-Gomes et al, 2005;Jørgensen and Mustafa, 1980;Lushchak et al, 1998), though its effect on mitochondrial enzymes is still debated (Hoppeler et al, 2003;Klimova and Chandel, 2008). Diet can have complex effects on metabolism, though the effects are most commonly seen in liver (de la Higuera et al, 1999;Hemre et al, 2002;LeMoine et al, 2008;Menoyo et al, 2004).…”