Ionoregulatory Aspects of the Osmorespiratory Compromise during Acute Environmental Hypoxia in 12 Tropical and Temperate Teleosts

Abstract

In the traditional osmorespiratory compromise, as seen in the hypoxia-intolerant freshwater rainbow trout (Oncorhynchus mykiss), the branchial modifications that occur to improve O2 uptake during hypoxia result in unfavorable increases in the fluxes of ions and water. However, at least one hypoxia-tolerant freshwater species, the Amazonian oscar (Astronotus ocellatus), shows exactly the opposite: decreased branchial flux rates of ions, water, and nitrogenous wastes during acute hypoxia. In order to find out whether the two strategies were widespread, we used a standard 2-h normoxia, 2-h hypoxia (20%-30% saturation), 2-h normoxic recovery protocol to survey 10 other phylogenetically diverse tropical and temperate species. Unidirectional influx and efflux rates of Na(+) and net flux rates of K(+), ammonia, and urea-N were measured. The flux reduction strategy was seen only in one additional species, the Amazonian tambaqui (Colossoma macropomum), which is similarly hypoxia tolerant and lives in the same ion-poor waters as the oscar. However, five other species exhibited evidence of the increased flux rates typical of the traditional osmorespiratory compromise in the trout: the rosaceu tetra (Hyphessobrycon bentosi rosaceus), the moenkhausia tetra (Moenkhausia diktyota), the bluegill sunfish (Lepomis macrochirus), the zebra fish (Danio rerio), and the goldfish (Carassius auratus). Four other species exhibited no marked flux changes during hypoxia: the cardinal tetra (Paracheirodon axelrodi), the hemigrammus tetra (Hemigrammus rhodostomus), the pumpkinseed sunfish (Lepomis gibbosus), and the Atlantic killifish (Fundulus heteroclitus). Overall, a diversity of strategies exist; we speculate that these may be linked to differences in habitat and/or lifestyle.

The transition from water-breathing to air-breathing is associated with a shift in ion uptake from gills to gut: a study of two closely related erythrinid teleosts, Hoplerythrinus unitaeniatus and Hoplias malabaricus

“…3): ions are lost as effective branchial permeability is increased in an attempt to acquire more O 2 from the environment (e.g. Randall et al 1972;Iftikar et al 2010;Robertson et al 2015). Jeju were able to avoid this effect (Fig.…”

Gill paracellular permeability and the osmorespiratory compromise during exercise in the hypoxia-tolerant Amazonian oscar (Astronotus ocellatus)

“…Nevertheless, oscars did exhibit increased unidirectional effluxes of Na + and net losses of K + during exercise (Fig. 3), in contrast to the decreases in these parameters seen during acute hypoxia (Wood et al 2007(Wood et al , 2009De Boeck et al 2013;Robertson et al 2015). During hypoxia, these flux reductions were attributed to decreased transcellular permeability associated with a rapid morphological response, a reduction in exposed MRC numbers and mean apical crypt surface areas due to a paving over by PVCs (Wood et al 2009;Matey et al 2011;De Boeck et al 2013).…”

“…5) may be an important factor explaining the low gill paracellular permeability. The ILCM may well be adaptive in reducing ionoregulatory and osmoregulatory costs in this species which lives in an ion-poor environment and which has relatively low metabolic rate (Sloman et al 2006), high blood O 2 affinity (Robertson et al 2015), and high hypoxia tolerance (Almeida- Val and Hochachka 1995;Muusze et al 1998;Almeida-Val et al 2000). In future studies, it will be of interest to see if the ILCM in the oscar decreases in volume, thereby allowing greater protrusion of the lamellae and increasing the surface area for gas exchange during prolonged hypoxia exposure or exercise, or at very high temperature, or if it proliferates at colder temperatures leaving shorter lamellae and decreasing the surface area of the gills.…”

“…To date, most studies have focused on the osmorespiratory compromise during swimming activity in highly aerobic fish such as salmonids, showing increased ion and water fluxes (Stevens 1972;Wood and Randall 1973a, b, c;Hofmann and Butler 1979;Wood 1988;McDonald 1992, 1994;Postlethwaite and McDonald 1995). Several studies have demonstrated comparable effects during hypoxia in salmonids (Thomas et al 1986;Iftikar et al 2010;Robertson et al 2015). It is usually assumed that most of these fluxes are occurring via the paracellular pathway, though this has not been directly demonstrated.…”

“…The first is the discovery of a freshwater fish, the Amazonian oscar (Astronotus ocellatus), which shows a very different response, a decrease in branchial ion and water fluxes during environmental hypoxia (Wood et al 2007(Wood et al , 2009Richards et al 2007;De Boeck et al 2013;Robertson et al 2015). This cichlid lives in ion-poor water and frequently encounters very low O 2 in its natural environment , tolerating levels of 5-20 % air saturation for 20-50 h and up to 6 h of complete anoxia (Almeida- Val and Hochachka 1995;Muusze et al 1998;Almeida-Val et al 2000).…”