Can variation among hypoxic environments explain why different fish species use different hypoxic survival strategies?

Abstract

In aquatic environments, hypoxia is a multi-dimensional stressor that can vary in O 2 level (partial pressure of O 2 in water, Pw O2), rate of induction and duration. Natural hypoxic environments can therefore be very different from one another. For the many fish species that have evolved to cope with these different hypoxic environments, survival requires adjusting energy supply and demand pathways to maintain energy balance. The literature describes innumerable ways that fishes combine aerobic metabolism, anaerobic metabolism and metabolic rate depression (MRD) to accomplish this, but it is unknown whether the evolutionary paths leading to these different strategies are determined primarily by species' phylogenetic histories, genetic constraint or their native hypoxic environments. We explored this idea by devising a four-quadrant matrix that bins different aquatic hypoxic environments according to their duration and Pw O2 characteristics. We then systematically mined the literature for well-studied species native to environments within each quadrant, and, for each of 10 case studies, described the species' total hypoxic response (THR), defined as its hypoxia-induced combination of sustained aerobic metabolism, enhanced anaerobic metabolism and MRD, encompassing also the mechanisms underlying these metabolic modes. Our analysis revealed that fishes use a wide range of THRs, but that distantly related species from environments within the same matrix quadrant have converged on similar THRs. For example, environments of moderately hypoxic Pw O2 favoured predominantly aerobic THRs, whereas environments of severely hypoxic Pw O2 favoured MRD. Capacity for aerial emergence as well as predation pressure (aquatic and aerial) also contributed to these responses, in addition to other biotic and abiotic factors. Generally, it appears that the particular type of hypoxia experienced by a fish plays a major role in shaping its particular THR.

The challenge of novel abiotic conditions for species undergoing climate‐induced range shifts

“…Consequently, tropical lake fish exhibit low thermal and hypoxia tolerance, and no acclimatization potential to changes expected in the future (McDonnell and Chapman 2015). By examining aquatic organisms living in four different hypoxia regimes, a recent study (Mandic and Regan 2018) investigated whether biogeographic history could better explain species‐specific physiological mechanisms, compared to phylogenetic predictions (Fig. 3).…”

“…The environment in which each organism lives better predicted the mechanisms used than did phylogenetic relationships, and these mechanisms were convergent across a broad variety of taxa. Adapted from Mandic and Regan (2018). Representative taxa for each order available in Supplementary material Appendix 1 Table A2.…”

Warming waters beget smaller fish: evidence for reduced size and altered morphology in a desert fish following anthropogenic temperature change

“…Measurements of dissolved O 2 (DO) in Tecopa Bore between 2014 and 2016 indicate DO is considerably lower in Tecopa Bore (1.82-3.63 mg l −1 ; 25.8-40.8% saturation) than in the Amargosa River (6.32-11.85 mg l −1 ; 62.6-68.6%). While it is not known if DO conditions changed in Tecopa Bore between 2008 and 2013-2014, or if consistent exposure to low DO alone can induce the development of morphological traits mirroring those observed for pupfish in Tecopa Bore, it is well established that hypoxia can depress metabolic rate [38] and increase the expression of less-efficient metabolic pathways involving anaerobic enzymes such as lactate dehydrogenase (LDH) [39,40], with responses varying both with hypoxia duration and taxonomically [41,42]. Muscle LDH activity measured in pupfish collected from Tecopa Bore in 2014 was approximately 2× higher than in conspecifics from the Amargosa River, suggesting heightened anaerobic capacity [43].…”

Oxygen Depletion Affects Kinematics and Shoaling Cohesion of Cyprinid Fish

“…Hypoxic events affect Mediterranean rivers worldwide [2,29], and fish, in particular, are highly sensitive to reduced oxygen concentrations [9,30]. The ecological impact of such events ranges from beneficial to mortality [31], but common responses include behavioral alterations [5,9,18].…”