Acid–base and ion balance in fishes with bimodal respiration

Abstract

The evolution of air breathing during the Devonian provided early fishes with bimodal respiration with a stable O2 supply from air. This was, however, probably associated with challenges and trade-offs in terms of acid-base balance and ionoregulation due to reduced gill:water interaction and changes in gill morphology associated with air breathing. While many aspects of acid-base and ionoregulation in air-breathing fishes are similar to water breathers, the specific cellular and molecular mechanisms involved remain largely unstudied. In general, reduced ionic permeability appears to be an important adaptation in the few bimodal fishes investigated but it is not known if this is a general characteristic. The kidney appears to play an important role in minimizing ion loss to the freshwater environment in the few species investigated, and while ion uptake across the gut is probably important, it has been largely unexplored. In general, air breathing in facultative air-breathing fishes is associated with an acid-base disturbance, resulting in an increased partial pressure of arterial CO2 and a reduction in extracellular pH (pHE ); however, several fishes appear to be capable of tightly regulating tissue intracellular pH (pHI ), despite a large sustained reduction in pHE , a trait termed preferential pHI regulation. Further studies are needed to determine whether preferential pHI regulation is a general trait among bimodal fishes and if this confers reduced sensitivity to acid-base disturbances, including those induced by hypercarbia, exhaustive exercise and hypoxia or anoxia. Additionally, elucidating the cellular and molecular mechanisms may yield insight into whether preferential pHI regulation is a trait ultimately associated with the early evolution of air breathing in vertebrates.

High capacity for extracellular acid-base regulation in the air-breathing fishPangasianodon hypophthalmus

“…This reveals a pronounced capacity for metabolic pH e regulation during hypercapnia in P. hypophthalmus. This is in stark contrast to all other air-breathing fishes studied to date that have a low capacity for pH e regulation during a respiratory acidosis (Shartau and Brauner, 2014). Thus, the armored catfish Liposarcus pardalis only recovered 8% and 22% of the pH e disturbance when exposed to ∼7 mmHg CO 2 and 42 mmHg CO 2 , respectively for 96 h (Brauner et al, 2004).…”

“…However, the gills of airbreathing fishes are generally reduced in size -an adaptation that is presumed to aid in avoiding branchial O 2 loss in hypoxic water -but have retained their ancestral function in acid-base and ion regulation (Graham, 1997;Tamura and Moriyama, 1976). It has therefore been suggested that the reduced surface area of the gills of air-breathing fishes places limitations on transepithelial ion exchange, thus constraining the branchial capacity for acid-base regulation (Brauner and Baker, 2009;Shartau and Brauner, 2014). Therefore, all studies on acid-base regulation in air-breathing fishes to date indicate a low capacity for exchange of acid-base equivalents in pH e regulation and a preferential regulation of intracellular pH, during a respiratory acidosis (Brauner and Baker, 2009;Brauner et al, 2004;Harter et al, 2014b;Heisler, 1982;Shartau and Brauner, 2014).…”

The amphibious fishKryptolebias marmoratususes alternate strategies to maintain oxygen delivery during aquatic hypoxia and air exposure

“…Impaired O 2 transport can also occur via the Root effect: a phenomenon found only in fishes, which prevents Hb from becoming fully O 2 saturated at high P CO 2 (Root and Irving, 1941;Gillen and Riggs, 1971). It has been hypothesized that welladapted air-breathing and amphibious fishes should possess relatively pH-insensitive Hb to reduce the consequences of Bohr and Root effects on O 2 transport (Graham, 1997;Shartau and Brauner, 2014); however, not all air-breathing fishes follow this pattern (e.g. Farmer et al, 1979;Wells et al, 1997).…”

Air breathing in the Arctic: influence of temperature, hypoxia, activity and restricted air access on respiratory physiology of Alaska blackfish (Dallia pectoralis)

“…That exercise, like increased temperature, did not induce air breathing might indicate that hypoxic stimulation of external rather than internal O 2 receptors is needed to initiate air breathing. It could also be an adaptive strategy that lowers the risk of aerial predation at a time when the fish has little capacity left for anaerobic burst swimming and thus escape responses, while also facilitating excretion of CO 2 (Shartau and Brauner, 2014). It would be interesting to investigate whether hypoxia restricts sustained swimming performance in Alaska blackfish, as observed in the banded knifefish (Gymnotus carapo) (McKenzie et al, 2012).…”