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

Abstract

Freshwater-and seawater-acclimated Fundulus heteroclitus were exposed to acute hypoxia (10% air saturation, 3 h), followed by normoxic recovery (3 h). In both salinities, ventilation increased and heart rate fell in the classic manner, while _ M O 2 initially declined by ∼50%, with partial restoration by 3 h of hypoxia, and no O 2 debt repayment during recovery. Gill paracellular permeability (measured with [ 14 C] PEG-4000) was 1.4-fold higher in seawater, and declined by 50% during hypoxia with post-exposure overshoot to 188%. A similar pattern with smaller changes occurred in freshwater. Drinking rate (also measured with [ 14 C] PEG-4000) was 8-fold higher in seawater fish, but declined by ∼90% during hypoxia in both groups, with post-exposure overshoots to ∼270%. Gill diffusive water flux (measured with 3 H 2 O) was 1.9-fold higher in freshwater fish, and exhibited a ∼35% decrease during hypoxia, which persisted throughout recovery, but was unchanged during hypoxia in seawater fish. Nevertheless, freshwater killifish gained mass while seawater fish lost mass during hypoxia, and these changes were not corrected during normoxic recovery. We conclude that this hypoxiatolerant teleost beneficially reduces gill water permeability in a salinity-dependent fashion during hypoxia, despite attempting to simultaneously improve _ M O 2 , but nevertheless incurs a net water balance penalty in both freshwater and seawater.

Linking environmental salinity to respiratory phenotypes and metabolic rate in fishes: a data mining and modelling approach

“…A salinity-specific effect on gill permeability has not been studied broadly, but data for a few species exist. FW-acclimated killifish have higher branchial water permeability than SW conspecifics, but they display similar diffusive ion fluxes (in opposite directions) during hypoxic hyperventilation (Giacomin et al, 2019;Wood et al, 2019). However, while FW-acclimated killifish do not alter ionocyte density, they do decrease their overall GSA (Giacomin et al, 2019), which is consistent with our observation of lower G d in FW fishes that may perhaps occur via different mechanisms in different species and conditions.…”

Gills versus kidney for ionoregulation in the obligate air-breathingArapaima gigas, a fish with a kidney in its air-breathing organ

“…5), with evidence of reduced water entry provided by reduced UFR (Fig. 2A)] all fit the response pattern seen in other hypoxia-tolerant teleosts where branchial fluxes of ions, water and ammonia are decreased by selective reductions in permeability and ion transport that do not appear to affect respiratory gas exchange (Wood et al, 2007(Wood et al, , 2009(Wood et al, , 2019Scott et al, 2008;Matey et al, 2011;De Boeck et al, 2013;Robertson et al, 2015;Giacomin et al, 2020). This is different from the traditional osmorespiratory compromise seen in fish that are not tolerant of hypoxia (Randall et al, 1972;Iftikar et al, 2010;Robertson et al, 2015).…”

“…2B), and a longer-lasting fall in U K (Table S3G). The fall in UFR has been seen previously in the Amazonian oscar (Wood et al, 2009) and may in fact be a consequence of a general reduction in gill permeability during aquatic hypoxia that has been reported in the oscar and in other species of hypoxia-tolerant but water-breathing fish (Wood et al, 2007(Wood et al, , 2019De Boeck et al, 2013;Robertson et al, 2015;Giacomin et al, 2020). Decreased permeability leads to decreased water entry, decreased GFR and decreased UFR.…”

“…Donald, 1989;Sundin and Nilsson, 2002;Marshall, 2003;Jonz and Zaccone, 2009) may be a more likely explanation, and could account for the persistent inhibition of branchial J Na,in during normoxic recovery. Indeed, there is precedence for such a long-lasting effect seen in a continuing reduction in gill water permeability of the freshwater killifish during 3 h of normoxic recovery after 3 h of severe aquatic hypoxia (10% air saturation; Wood et al, 2019).…”

Rapid and reversible modulation of blood haemoglobin content during diel cycles of hypoxia in killifish (Fundulus heteroclitus)

“…It is unlikely that erythrocyte swelling contributed to the haematological changes in killifish reported here because there were no observed alterations in mean-cell haemoglobin content (Table 1). Reductions in plasma volume could result from increases in blood pressure in hypoxia that increase capillary filtration (Hedrick et al, 2020;Pearson and Stevens, 1991), but this effect would likely be opposed by osmotic water gains that killifish experience during hypoxia exposure in hypo-osmotic environments and would tend to increase extracellular fluid volume (Wood et al, 2019). If reductions in plasma volume occur despite these potential increases in extracellular fluid volume, reductions in plasma volume might have contributed to some of the increase in blood haemoglobin content that remained unexplained by splenic contraction.…”