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

Abstract

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

Amphibious fishes: evolution and phenotypic plasticity

“…In terrestrial lungfish (Protopterus dolloi), whole-body water efflux decreased substantially by 1 week and remained low over 6 months out of water (Wilkie et al, 2007). Similarly, in the non-aestivating K. marmoratus, whole-body water efflux was lower during emersion over a hypersaline (45 ppt; mimics seasonal drought) but not hyposaline (1 ppt) substrate .…”

“…Amphibious fishes may be tolerant of some water loss for intervals when they emerse (Horn and Gibson, 1988;Evans et al, 1999), but many have strategies to remain in positive water balance (e.g. Litwiller et al, 2006;Wilkie et al, 2007;Frick et al, 2008a). Behavioural strategies are often used to limit water loss and maintain hydration in fish out of water.…”

“…For example, in marine Periophthalmodon schlosseri and freshwater marble goby, Oxyeleotris marmorata, held out of water for 6 h, Ca 2+ homeostasis was maintained by a large decrease in cutaneous Ca 2+ efflux to almost zero (Fenwick and Lam, 1988). Over longer periods of emersion, however, other species show little change in whole-body flux rates for Na + and Cl Wilkie et al, 2007;K. marmoratus, LeBlanc et al, 2010).…”

Increased gene expression of a facilitated diffusion urea transporter in the skin of the African lungfish (Protopterus annectens) during massively elevated post-terrestrialization urea excretion

“…In the experimental series of the present study, some of the lungfish were subjected to an experimental treatment similar to that employed by Wood and colleagues (Wood et al, 2005) and Wilkie and colleagues (Wilkie et al, 2007). This was originally described as 'terrestrialization' by Wood and colleagues (Wood et al, 2005) and the same term is used here; it should not be confused with true 'aestivation' (see Loong et al, 2008).…”

“…While submerged in water, lungfishes are usually ammoniotelic, producing ammonia and excreting it across branchial and cutaneous epithelia (Graham, 1997;Wood et al, 2005). However, when water becomes limited and ammonia excretion becomes impeded, lungfishes convert toxic ammonia into a less toxic nitrogenous product, urea, and store it in the body (Smith, 1930;Janssens, 1964;DeLaney et al, 1974;Chew et al, 2003;Chew et al, 2004;Wood et al, 2005;Ip et al, 2005;Loong et al, 2005;Loong et al, 2008;Wilkie et al, 2007).…”