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

Abstract

In the traditional osmorespiratory compromise, fish increase their effective gill permeability to O2 during exercise or hypoxia, and in consequence suffer unfavorable ionic and osmotic fluxes. However oscars, which live in the frequently hypoxic ion-poor waters of the Amazon, actually decrease ionic fluxes across the gills during acute hypoxia without changing gill paracellular permeability, and exhibit rapid paving over of the mitochondrial-rich cells (MRCs). But what happens during prolonged exercise? Gill paracellular permeability, ionic fluxes, and gill morphology were examined in juvenile oscars at rest and during aerobic swimming. Initial validation tests with urinary catheterized fish quantified drinking, glomerular filtration, and urinary flow rates, and confirmed that measurements of gill paracellular permeability as [(3)H]PEG-4000 clearances were the same in efflux and influx directions, but far lower than previously measured in comparably sized trout. Although the oscars achieved a very similar proportional increase (90%) in oxygen consumption (MO2) to trout during steady-state swimming at 1.2 body lengths sec(-1), there was no increase in gill paracellular permeability, in contrast to trout. However, oscars did exhibit increased unidirectional Na(+) efflux and net K(+) rates during exercise, but no change in drinking rate. There were no changes in MRC numbers or exposure, or other alterations in gill morphology during exercise. A substantial interlamellar cell mass (ILCM) that covered the lamellae to a depth of 30% was unchanged by 4 h of swimming activity. We conclude that a low branchial paracellular permeability which can be dissociated from changes in O2 flux, as well as the presence of the ILCM, may be adaptive in limiting ionoregulatory costs for a species endemic to ion-poor, frequently hypoxic waters.

The osmorespiratory compromise in the euryhaline killifish: water regulation during hypoxia

“…Wood and Marshall, 1994;Wilson and Laurent, 2002) and the observation that the expression levels of claudins are generally lower in the gills of seawater-adapted fish (Chasiotis et al, 2012), including F. heteroclitus (Whitehead et al, 2010(Whitehead et al, , 2011. There are only a few previous measurements of PEG-4000 permeability in fish gills, all in freshwater (Scott et al, 2004;Sloman et al, 2004;Robertson and Wood, 2014;Robertson et al, 2015a). The present C PEG values are the lowest yet recorded, indeed approximately 65% below the earlier low values of Scott et al (2004) for the same species.…”

“…Clearly, C PEG reflects a different pathway from k 3H2O . To our knowledge, the present data provide the first evidence that gill paracellular permeability can be altered by acute changes in O 2 availability, though it increases with exercise in the trout (Robertson and Wood, 2014), but not in the oscar (Robertson et al, 2015a). One possible control is the stress hormone cortisol, which is known to increase during acute hypoxia (Mommsen et al, 1999) and to decrease gill paracellular permeability through effects on tight junctions (Chasiotis et al, 2012).…”

“…Interestingly, neither the killifish (Fig. 3) nor the oscar (Robertson et al, 2015a) showed this osmorespiratory compromise during exercise, suggesting that the response is specific to hypoxia in these hypoxia-tolerant species. In the hypoxiaintolerant trout, exactly the opposite occurred during hypoxia: increased k 3H2O , increased ion fluxes and uncovering of the chloride cells (Iftikar et al, 2010;Matey et al, 2011;Robertson et al, 2015b), though the increased k 3H2O was attenuated over time (Onukwufor and Wood, 2018).…”

“…The compromise has been documented most extensively with respect to increased ion loss accompanying exercise in freshwater fish, when O 2 demand increases (e.g. Wood and Randall, 1973a,b;McDonald, 1992, 1994;Wood, 1988;Postlethwaite and McDonald, 1995;Robertson and Wood, 2014;Robertson et al, 2015a;Onukwufor and Wood, 2018). There have been fewer studies on the compromise with respect to increased water exchange during exercise (Stevens, 1972;Wood and Randall, 1973c;Hofmann and Butler, 1979;Wood, 1988;Onukwufor and Wood, 2018), and almost none on seawater fish (Farmer and Beamish, 1969;Stevens, 1972).…”

The effects of hypoxia on active ionic transport processes in the gill epithelium of hyperregulating crab, Carcinus maneas

“…Upon reoxygenation Na + uptake was recovered. The low branchial paracellular permeability tested during swimming exercise may be an additional adaptive mechanism in limiting osmoregulatory cost under hypoxia (Wood et al, 2007;Robertson et al, 2015). Hypoxia diminishes intracellular ATP production in the trout hepatocytes (Bogdanova et al, 2005).…”