Greatly Elevated Urea Excretion after Air Exposure Appears to Be Carrier Mediated in the Slender Lungfish (<i>Protopterus dolloi</i>)

Wood, Chris M.; Walsh, Patrick J.; Chew, Shit F.; Ip, Yuen K.

doi:10.1086/432919

Cited by 35 publications

(49 citation statements)

References 56 publications

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“…Plasma urea concentrations in aquatic P. dolloi were comparable with concentrations in previous studies on this species (Lim et al 2004;Ip et al 2005;Wood et al 2005) as well as P. aethiopicus (Smith 1930;DeLaney et al 1977;Loong et al 2005) and Protopterus annectens . The magnitude of plasma urea elevation was comparable with increases previously reported in this species during air exposure (Ip et al ).…”

Section: The Slender African Lungfish Maintains Osmotic and Electrolysupporting

confidence: 82%

“…2005; Wood et al 2005) but less than in other species of estivating Protopterus (Smith 1930;Janssens 1964;DeLaney et al 1977;Ip et al 2005). The accumulation of urea may not have been as great in our study as in fully estivating lungfish due to extrabranchial urea excretion.…”

Section: The Slender African Lungfish Maintains Osmotic and Electrolycontrasting

confidence: 58%

“…With the onset of the dry season, some lungfish burrow into the mud and secrete a mucus cocoon that surrounds the body to reduce desiccation (see Fishman et al 1986 for review). During both estivation and air exposure, nitrogenous wastes are also converted to and stored in the body as urea, rather than as the more toxic ammonia (Smith 1930(Smith , 1931Janssens 1964;Jans-sens and Cohen 1968;DeLaney et al 1974DeLaney et al , 1977Chew et al 2003Chew et al , 2004Loong et al 2005;Wood et al 2005). Only P. annectens is reported to estivate in nature on a regular basis (Greenwood 1986), but all African lungfish have the ability to secrete a cocoon and to enter an estivation-like state when denied access to water in the laboratory.…”

Section: Introductionmentioning

confidence: 99%

“…An ability to continue uptake of water and/or ions from the limited water remaining in their habitat by using other routes/mechanisms could therefore prolong lungfish survival by minimizing the severity of osmotic and ionic disturbances. To examine this possibility, we took advantage of the ability of P. dolloi to survive out of water for prolonged periods by entering an estivation-like state characterized by the secretion of a cocoon that envelops the animal's dorsolateral body surface while the ventral surface remains in contact with the moist substrate (Chew et al 2003;Wood et al 2005). Because humid conditions are essential for survival under such circumstances, we predicted that water and ion uptake would take place across the ventral body surface.…”

Section: Introductionmentioning

confidence: 99%

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The African Lungfish (Protopterus dolloi): Ionoregulation and Osmoregulation in a Fish out of Water

Wilkie

Morgan

Gálvez

et al. 2007

Physiological and Biochemical Zoology

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Although urea production and metabolism in lungfish have been thoroughly studied, we have little knowledge of how internal osmotic and electrolyte balance are controlled during estivation or in water. We tested the hypothesis that, compared with the body surface of teleosts, the slender African lungfish (Protopterus dolloi) body surface was relatively impermeable to water, Na ϩ , and Cl Ϫ due to its greatly reduced gills. Accordingly, we measured the tritiated water ( 3 H-H 2 O) flux in P. dolloi in water and during air exposure. In water, 3 H-H 2 O efflux was comparable with the lowest measurements reported in freshwater teleosts, with a rate constant (K) of 17.6% body water h Ϫ1 . Unidirectional ion fluxes, measured using 22 Na ϩ and 36 Cl Ϫ , indicated that Na ϩ and Cl Ϫ influx was more than 90% lower than values reported in most freshwater teleosts. During air exposure, a cocoon formed within 1 wk that completely covered the dorsolateral body surface. However, there were no disturbances to blood osmotic or ion (Na ϩ , Cl Ϫ ) balance, despite seven-to eightfold increases in plasma urea after 20 wk. Up to 13-fold increases in muscle urea (on a dry-weight basis) were the likely explanation for the 56% increase in muscle water * Corresponding author. Address for correspondence: Department of Biology, Wilfrid Laurier University, 75 University Avenue West, Waterloo, Ontario N2L 3C5, Canada; e-mail: mwilkie@wlu.ca. content observed after 20 wk of air exposure. The possibility that muscle acted as a "water reservoir" during air exposure was supported by the 20% decline in body mass observed during subsequent reimmersion in water. This decline in body mass was equivalent to 28 mL water in a 100-g animal and was very close to the calculated net water gain (approximately 32 mL) observed during the 20-wk period of air exposure. Tritiated water and unidirectional ion fluxes on air-exposed lungfish revealed that the majority of water and ion exchange was via the ventral body surface at rates that were initially similar to aquatic rates. The 3 H-H 2 O flux declined over time but increased upon reimmersion. We conclude that the slender lungfish body surface, including the gills, has relatively low permeability to water and ions but that the ventral surface is an important site of osmoregulation and ionoregulation. We further propose that an amphibian-like combination of ventral skin water and ion permeability, plus internal urea accumulation during air exposure, allows P. dolloi to extract water from its surroundings and to store water in the muscle when the water supply becomes limited. Physiological and Biochemical Zoology

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Section: The Slender African Lungfish Maintains Osmotic and Electrolysupporting

confidence: 82%

Section: The Slender African Lungfish Maintains Osmotic and Electrolycontrasting

confidence: 58%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The African Lungfish (Protopterus dolloi): Ionoregulation and Osmoregulation in a Fish out of Water

Wilkie

Morgan

Gálvez

et al. 2007

Physiological and Biochemical Zoology

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“…On day 3, the Wsh was exposed to air and on day 6 the Wsh would have entered into aestivation with the formation of a completely dried mucus cocoon. Contrary to the proposition of Perry et al (2008), these experimental Wsh cannot be regarded as undergoing "terrestrialization", because no water was added to prevent the formation of a completely dried cocoon as in the case of series two experiment performed by Wood et al (2005). Since we could induce P. annectens to aestivate in air-tight plastic boxes, we were able to determine for the Wrst time ATP and creatine phosphate concentrations in various regions of the live Wsh during 12 days of induction and maintenance of aestivation using in vivo 31 P NMR spectroscopy.…”

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confidence: 98%

Effects of hypoxia on the energy status and nitrogen metabolism of African lungfish during aestivation in a mucus cocoon

et al. 2008

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We examined the energy status, nitrogen metabolism and hepatic glutamate dehydrogenase activity in the African lungWsh Protopterus annectens during aestivation in normoxia (air) or hypoxia (2% O 2 in N 2 ), with tissues sampled on day 3 (aerial exposure with preparation for aestivation), day 6 (entering into aestivation) or day 12 (undergoing aestivation). There was no accumulation of ammonia in tissues of Wsh exposed to normoxia or hypoxia throughout the 12-day period. Ammonia toxicity was avoided by increased urea synthesis and/or decreased endogenous N production (as ammonia), but the dependency on these two mechanisms diVered between the normoxic and the hypoxic Wsh. The rate of urea synthesis increased 2.4-fold, with only a 12% decrease in the rate of N production in the normoxic Wsh. By contrast, the rate of N production in the hypoxic Wsh decreased by 58%, with no increase in the rate of urea synthesis. Using in vivo 31 P NMR spectroscopy, it was demonstrated that hypoxia led to signiWcantly lower ATP concentration on day 12 and signiWcantly lower creatine phosphate concentration on days 1, 6, 9 and 12 in the anterior region of the Wsh as compared with normoxia. Additionally, the hypoxic Wsh had lower creatine phosphate concentration in the middle region than the normoxic Wsh on day 9. Hence, lowering the dependency on increased urea synthesis to detoxify ammonia, which is energy intensive by reducing N production, would conserve cellular energy during aestivation in hypoxia. Indeed, there were signiWcant increases in glutamate concentrations in tissues of Wsh aestivating in hypoxia, which indicates decreases in its degradation and/or transamination. Furthermore, there were signiWcant increases in the hepatic glutamate dehydrogenase (GDH) amination activity, the amination/deamination ratio and the dependency of the amination activity on ADP activation in Wsh on days 6 and 12 in hypoxia, but similar changes occurred only in the normoxic Wsh on day 12. Therefore, our results indicate for the Wrst time that P. annectens exhibited diVerent adaptive responses during aestivation in normoxia and in hypoxia. They also indicate that reduction in nitrogen metabolism, and probably metabolic rate, did not occur simply in association with aestivation (in normoxia) but responded more eVectively to a combined eVect of aestivation and hypoxia.

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Renal Corpuscle of the African Lungfish Protopterus dolloi: Structural and Histochemical Modifications During Aestivation

Ojeda

Wong

et al. 2008

The Anatomical Record

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This work studies the structural and lectin-binding modifications experienced by the renal corpuscle of the African lungfish Protopterus dolloi during aestivation. The kidney of the aestivating animals was studied by light-and electron-microscopy, and by immunofluorescence methods. Upon aestivation, the renal corpuscles (RCs) undergo a marked size reduction, and all the structural RC components are affected. The parietal cells of Bowman's capsule lose their flattened appearance and adopt the organization of a stratified epithelium. The glomerular capillaries collapse. The podocytes approach each other. Concomitantly, the major processes between contiguous cells are lost, the rest of the major processes adopting a lamina-like configuration. The foot processes lose their regular arrangement, the filtration slits are difficult to observe, and the subpodocyte space disappears. The glomerular basement membrane (GBM) thickens enormously, increases the amount of amorphous material and of collagen, and round inclusions formed by amorphous material and coiled fibrils appear. The mesangial cells compact and form a dense network embedded in the subendothelial lamina of the GBM. The endothelial cells show numerous irregularities, establishing abnormal interrelationships with the mesangial cells. These modifications are accompanied by changes in the expression of the carbohydrate moieties, as indicated by the modifications in lectin-binding patterns. On the whole, these modifications thicken and compact the filtration barrier, thus reducing the filtration coefficient and allowing the organism to cope with dehydration. All these modifications are partially reversed during the first days of returning the animals to freshwater. The renal corpuscle appears to be a highly dynamic structure capable of modifying its architecture in response to environmental changes. Anat

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Greatly Elevated Urea Excretion after Air Exposure Appears to Be Carrier Mediated in the Slender Lungfish (Protopterus dolloi)

Cited by 35 publications

References 56 publications

The African Lungfish (Protopterus dolloi): Ionoregulation and Osmoregulation in a Fish out of Water

The African Lungfish (Protopterus dolloi): Ionoregulation and Osmoregulation in a Fish out of Water

Effects of hypoxia on the energy status and nitrogen metabolism of African lungfish during aestivation in a mucus cocoon

Renal Corpuscle of the African Lungfish Protopterus dolloi: Structural and Histochemical Modifications During Aestivation

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