Air breathing in Magadi tilapia Alcolapia grahami, under normoxic and hyperoxic conditions, and the association with sunlight and reactive oxygen species

Abstract

Observations of the Magadi tilapia Alcolapia grahami in hot, highly alkaline Lake Magadi revealed that they air breathe not only during hypoxia, as described previously, but also during normoxia and hyperoxia. Air breathing under these latter conditions occurred within distinct groupings of fish (pods) and involved only a small proportion of the population. Air breathing properties (duration and frequency) were quantified from video footage. Air breathing within the population followed a diel pattern with the maximum extent of pod formation occurring in early afternoon. High levels of reactive oxygen species (ROS) in the water may be an irritant that encourages the air-breathing behaviour. The diel pattern of air breathing in the field and in experiments followed the diel pattern of ROS concentrations in the water which are amongst the highest reported in the literature (maximum daytime values of 2.53 – 8.10 μM H₂O₂). Interlamellar cell masses (ILCM) occurred between the gill lamellae of fish from the lagoon with highest ROS and highest oxygen levels, while fish from a normoxic lagoon with one third the ROS had little or no ILCM. This is the first record of air breathing in a facultative air-breathing fish in hyperoxic conditions and the first record of an ILCM in a cichlid species.

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).…”

Genomics of Adaptation to Multiple Concurrent Stresses: Insights from Comparative Transcriptomics of a Cichlid Fish from One of Earth’s Most Extreme Environments, the Hypersaline Soda Lake Magadi in Kenya, East Africa

“…Members of the CYP family (including CYP3A40 with the highest dN/dS of 2.606 in our study) have been associated with detoxification processes such as in the European eel (Pujolar et al 2012). Owing to high levels of ROS and other free radicals associated with numerous stresses in Lake Magadi (Johannsson et al 2014), genes that promote their destruction would be selectively propagated in the genome.…”

“…These genes are involved in various metabolic activities including oxidative, peroxidative, and reductive metabolism of endogenous and exogenous substrates (Danielson 2002). Lake Magadi is a closed lake in which intensive ultraviolet radiation, high salinity, high pH, and high alkalinity, together with daytime hyperoxia synergize to produce high concentrations of ROS (Johannsson et al 2014).…”

“…1a). As in most endorbeic soda lakes, Lake Magadi is characterized by extreme environmental conditions: high levels of pH (up to 10), alkalinity, salinity, temperature (up to 40 °C), reactive oxygen species (ROS), and ultraviolet radiation, plus extreme daily fluctuations in oxygen concentration (Coe 1966;Narahara et al 1996;Johannsson et al 2014). This unusually stressful environment poses several physiological challenges.…”

“…In A. grahami, several behavioral and physiological adaptations to its challenging habitat have been described. These include air breathing as a mitigation mechanism against recurring hypoxic conditions, excretion of nitrogen in form of urea (as opposed to ammonia excreted by almost all other teleosts), high metabolic rates, and tolerance to high water alkalinity facilitated by a high pH in blood and tissues Randall et al 1989;Wood et al 1989;Portner et al 2010;Johannsson et al 2014).…”