Renal function and acid–base regulation in two Amazonian erythrinid fishes: <i>Hoplias malabaricus</i>, a water breather, and <i>Hoplerythrinus unitaeniatus</i>, a facultative air breather

Cameron, James N.; Wood, Chris M.

doi:10.1139/z78-127

Cited by 57 publications

(25 citation statements)

References 19 publications

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“…Ion losses through the kidney were not measured in the present study. However, Cameron and Wood (1978) directly cannulated the urinary papilla to collect excreted urine in these same two species, and reported that under normoxia, urinary Na + and Cl − efflux rates were significantly higher in the jeju, but amounted to only 10 % of the unidirectional Na + efflux rates at the gills in the jeju, and only 4 % in the traira. Thus the kidney appears to play at most a small role in the difference between the species.…”

Section: Branchial Ionoregulationmentioning

confidence: 99%

“…2) must have exceeded unidirectional influx rates at the gills in the jeju (and vice versa in the traira), but it is unclear whether the inter-species differences were due to higher active branchial influx rates, lower passive branchial efflux rates, or both, in the traira versus the jeju. Cameron and Wood (1978) reported no differences in either branchial Na + influx or efflux rates between the two species, but did not control feeding and worked on cannulated animals held in water containing about tenfold higher ion levels, so direct comparisons cannot be made. Based on the approximately 50 % smaller measured gill surface area and size in the jeju (Hulbert et al 1978b;Cameron and Wood 1978;Fernandes et al 1994), and the qualitative conclusion of Hulbert et al (1978a) that mitochondrial-rich cells are less abundant in the gills of the jeju, it seems likely that active unidirectional Na + and Cl − influx rates would also be lower in this species.…”

Section: Branchial Ionoregulationmentioning

confidence: 99%

“…Cameron and Wood (1978) reported no differences in either branchial Na + influx or efflux rates between the two species, but did not control feeding and worked on cannulated animals held in water containing about tenfold higher ion levels, so direct comparisons cannot be made. Based on the approximately 50 % smaller measured gill surface area and size in the jeju (Hulbert et al 1978b;Cameron and Wood 1978;Fernandes et al 1994), and the qualitative conclusion of Hulbert et al (1978a) that mitochondrial-rich cells are less abundant in the gills of the jeju, it seems likely that active unidirectional Na + and Cl − influx rates would also be lower in this species. However, we were surprised to find that branchial Na + ,K + ATPase activities were 3.5-fold higher, and branchial v-type H + ATPase activities were 1.6-fold higher in the jeju (both expressed per mg protein; Table 3).…”

Section: Branchial Ionoregulationmentioning

confidence: 99%

“…We chose two erythrinids, the jeju (Hoplerythrinus unitaeniatus), and the traira (Hoplias malabaricus), which have been studied as comparators previously (Cameron and Wood 1978;Driedzic et al 1978;Hulbert et al 1978a, b;Phleger and Saunders 1978;Stevens and Holeton 1978;Fernandes et al 1994;Perry et al 2004;Pelster et al submitted). The gills of the two species have been studied in detail previously: these investigations have confirmed that the mass-specific branchial surface area (Cameron and Wood 1978;Fernandes et al 1994) and the mass-specific weight of the gills (Hulbert et al 1978b) are both twice as large in the traira (the water-breather) as those in the jeju (the air-breather). Both have a physostomous swimbladder, but in the jeju the anterior portion of the posterior chamber is heavily vascularized (red in colour) whereas in the traira, the whole swimbladder is poorly vascularized (uniformly white in colour).…”

Section: Introductionmentioning

confidence: 99%

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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

et al. 2016

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The evolutionary transition from water-breathing to air-breathing involved not only a change in function of the organs of respiratory gas exchange and N-waste excretion, but also in the organs of ion uptake from the environment. A combination of in vivo and in vitro techniques was used to look at the relative importance of the gills versus the gut in Na(+), Cl(-), and K(+) balance in two closely related erythrinid species: a facultative air-breather, the jeju (Hoplerythrinus unitaeniatus) and an obligate water-breather, the traira (Hoplias malabaricus). The jeju has a well-vascularized physostomous swimbladder, while that in the traira is poorly vascularized, but the gills are much larger. Both species are native to the Amazon and are common in the ion-poor, acidic blackwaters of the Rio Negro. Under fasting conditions, the traira was able to maintain positive net Na(+) and Cl(-) balance in this water, and only slightly negative net K(+) balance. However, the jeju was in negative net balance for all three ions and had lower plasma Na(+) and Cl(-) concentrations, despite exhibiting higher branchial Na(+), K(+)ATPase and v-type H(+)ATPase activities. In the intestine, activities of these same enzymes were also higher in the jeju, and in vitro measurements of net area-specific rates of Na(+), Cl(-), and K(+) absorption, as well as the overall intestinal absorption capacities for these three ions, were far greater than in the traira. When acutely exposed to disturbances in water O2 levels (severe hypoxia ~15% or hyperoxia ~420% saturation), gill ionoregulation was greatly perturbed in the traira but less affected in the jeju, which could "escape" the stressor by voluntarily air-breathing. We suggest that a shift of ionoregulatory capacity from the gills to the gut may have occurred in the evolutionary transition to air-breathing in jeju, and in consequence branchial ionoregulation, while less powerful, is also less impacted by variations in water O2 levels.

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Section: Branchial Ionoregulationmentioning

confidence: 99%

Section: Branchial Ionoregulationmentioning

confidence: 99%

Section: Branchial Ionoregulationmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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

et al. 2016

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“…While this hypothesis has been investigated in facultative (Cameron and Wood, 1978) and obligate (reviewed by Graham, 1997) air-breathers with mixed findings, the greatest support has been obtained in comparisons among A. gigas and O. bicirrhosum. Estimates of ion-regulatory capacity, based upon measurements of gill and kidney masses and their respective homogenate Na + /K + -ATPase and Ca 2+ -ATPase activities Hulbert et al, 1978), indicate that the kidney may play a much greater role in A. gigas than in O. bicirrhosum; however, no in vivo physiological data presently exist to support or refute this hypothesis.…”

Section: Transition Of Branchial Physiological Function To the Kidneymentioning

confidence: 99%

Transition in organ function during the evolution of air-breathing;insights from Arapaima gigas, an obligate air-breathing teleost from the Amazon

Brauner

Matey

Wilson

et al. 2004

Journal of Experimental Biology

112

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SUMMARY The transition from aquatic to aerial respiration is associated with dramatic physiological changes in relation to gas exchange, ion regulation,acid–base balance and nitrogenous waste excretion. Arapaima gigas is one of the most obligate extant air-breathing fishes,representing a remarkable model system to investigate (1) how the transition from aquatic to aerial respiration affects gill design and (2) the relocation of physiological processes from the gills to the kidney during the evolution of air-breathing. Arapaima gigas undergoes a transition from water-to air-breathing during development, resulting in striking changes in gill morphology. In small fish (10 g), the gills are qualitatively similar in appearance to another closely related water-breathing fish (Osteoglossum bicirrhosum); however, as fish grow (100–1000 g), the inter-lamellar spaces become filled with cells, including mitochondria-rich(MR) cells, leaving only column-shaped filaments. At this stage, there is a high density of MR cells and strong immunolocalization of Na+/K+-ATPase along the outer cell layer of the gill filament. Despite the greatly reduced overall gill surface area, which is typical of obligate air-breathing fish, the gills may remain an important site for ionoregulation and acid–base regulation. The kidney is greatly enlarged in A. gigas relative to that in O. bicirrhosum and may comprise a significant pathway for nitrogenous waste excretion. Quantification of the physiological role of the gill and the kidney in A. gigas during development and in adults will yield important insights into developmental physiology and the evolution of air-breathing.

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Renal regulation of acid‐base balance in a freshwater fish

Wood

Caldwell

1978

J. Exp. Zool.

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Intra-arterial injection of a fixed acid load caused only a short-lived (less than 2h) disturbance of blood pH but a long lived (2-3 days) elevation of urinary acid excretion in freshwater trout (Salmo gairdneri). The renal response comprised an immediate increase in acid output in the form of titratable acidity minus bicarbonate, and a slower rise in acid output in the form of ammonia. The total elevation in urinary acid efflux over 72h was such that no other mechanism besides renal function is needed to explain the ultimate compensation of this experimental acid-base disturbance.

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Renal function and acid–base regulation in two Amazonian erythrinid fishes: Hoplias malabaricus, a water breather, and Hoplerythrinus unitaeniatus, a facultative air breather

Cited by 57 publications

References 19 publications

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

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

Transition in organ function during the evolution of air-breathing;insights from Arapaima gigas, an obligate air-breathing teleost from the Amazon

Renal regulation of acid‐base balance in a freshwater fish

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