Interspecific and environment-induced variation in hypoxia tolerance in sunfish

Borowiec, Brittney G.; Crans, Kyle; Khajali, Fariborz; Pranckevicius, Nicole A.; Young, A. P.; Scott, Graham R.

doi:10.1016/j.cbpa.2016.04.010

Cited by 27 publications

(23 citation statements)

References 84 publications

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“…The pumpkinseed's greater tolerance does not appear to result from greater aerobic abilities, as the two species do not differ in P crit (Mathers et al, 2014;Borowiec et al, 2016) or a wide array of underlying mechanisms (Crans et al, 2015;Borowiec et al, 2016). Where the species do differ is in their capacities for anaerobic metabolism, with the more tolerant pumpkinseed displaying higher lactate dehydrogenase activities in axial muscle (Farwell et al, 2007;Borowiec et al, 2016) and heart (Borowiec et al, 2016) than the less tolerant bluegill. The pumpkinseed's greater anaerobic capacity may contribute to its greater hypoxia tolerance, but because anaerobic glycolysis on its own is a limited long-term strategy owing to glycogen depletion and end-product accumulation, it is unlikely to solely explain how pumpkinseed can tolerate the more hypoxic northern lakes that bluegill cannot.…”

Section: Oligotrophic Winterfreeze Lakesmentioning

confidence: 99%

“…The ranges of two closely related sunfish, the bluegill (Lepomis macrochirus) and pumpkinseed (Lepomis gibbosus), overlap, but the most northern lakesthe ones that experience the most severe winterfreeze hypoxiacontain only pumpkinseed (Mittelbach, 1984;Farwell et al, 2007). Unsurprisingly, pumpkinseed have repeatedly been shown to be more hypoxia-tolerant than bluegill (Farwell et al, 2007;Mathers et al, 2014;Borowiec et al, 2016). The pumpkinseed's greater tolerance does not appear to result from greater aerobic abilities, as the two species do not differ in P crit (Mathers et al, 2014;Borowiec et al, 2016) or a wide array of underlying mechanisms (Crans et al, 2015;Borowiec et al, 2016).…”

Section: Oligotrophic Winterfreeze Lakesmentioning

confidence: 99%

“…Unsurprisingly, pumpkinseed have repeatedly been shown to be more hypoxia-tolerant than bluegill (Farwell et al, 2007;Mathers et al, 2014;Borowiec et al, 2016). The pumpkinseed's greater tolerance does not appear to result from greater aerobic abilities, as the two species do not differ in P crit (Mathers et al, 2014;Borowiec et al, 2016) or a wide array of underlying mechanisms (Crans et al, 2015;Borowiec et al, 2016). Where the species do differ is in their capacities for anaerobic metabolism, with the more tolerant pumpkinseed displaying higher lactate dehydrogenase activities in axial muscle (Farwell et al, 2007;Borowiec et al, 2016) and heart (Borowiec et al, 2016) than the less tolerant bluegill.…”

Section: Oligotrophic Winterfreeze Lakesmentioning

confidence: 99%

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

Mandic

Regan

2018

Journal of Experimental Biology

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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.

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Section: Oligotrophic Winterfreeze Lakesmentioning

confidence: 99%

Section: Oligotrophic Winterfreeze Lakesmentioning

confidence: 99%

Section: Oligotrophic Winterfreeze Lakesmentioning

confidence: 99%

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

Mandic

Regan

2018

Journal of Experimental Biology

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“…Several studies dealing with hybridization and the energy cost of this process have suggested a possible link between oxidative stress and increased metabolism observed in some hybrids (Gvoždík, 2012;Borowiec et al, 2016). Hybrids of the marine copepod (Tigriopus californicus) had elevated levels of DNA oxidative damage (higher levels of 8-OH-dG) than parental lines as a consequence either of increased basal ROS leakage due to a dysfunctional OXPHOS system, or from a reduced anti-oxidant capacity (Barreto and Burton, 2013).…”

Section: Oxidative Stress As the Cost Of Hybridizationmentioning

confidence: 99%

Oxidative cost of interspecific hybridization: a case study of two Triturus species and their hybrids

Prokić

Despotović

Vučić

et al. 2018

Journal of Experimental Biology

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Oxidative stress has most recently been suggested as one of the possible mechanisms responsible for reduced fitness of hybrids. To explore possible oxidative cost of hybridization, we examined anti-oxidant defence system parameters (superoxide dismutase, catalase, glutathione peroxidase, glutathione -transferase, glutathione reductase, glutathione, SH groups), their interconnectedness (index of integration) and levels of oxidative damage [concentrations of lipid peroxides, TBARS (thiobarbituric acid reactive substances)] in laboratory-reared newt species, and , and their hybrid. Our results showed that parental species differed in anti-oxidant defence system parameters, but not in the levels of integration of the whole system and oxidative damage. Individuals of had higher activities of superoxide dismutase, glutathione -transferase and concentrations of glutathione. Hybrid individuals of crested newts displayed higher levels of the anti-oxidant defence system (higher superoxide dismutase, catalase, glutathione peroxidase activities and concentrations of SH groups), and a lower overall correlation of anti-oxidant system (lower index of integration) in comparison with both parental species, suggesting that they may possess a less efficient anti-oxidant defence system and a higher investment in maintaining oxidative balance. The higher investment in the anti-oxidant system could divert limited resources away from other functions and affect further hybrid fitness. The presented findings contribute to a better understanding of the anti-oxidant defence system of crested newts and their interspecies differences, and support the hypothesis that oxidative stress is one of the costs of interspecific hybridization.

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“…These lamellae are the main site of exchange between the fish and environment due to their large total surface area and very short water-blood diffusion distances [1,2]. Athletic or hypoxia-tolerant fishes tend to have large gills relative to their body mass, while sluggish fishes have less gill surface area [2][3][4][5]. The importance of gill size to the respiratory capacity of fishes has even led to the recent hypothesis that the adaptive responses of fishes to climate change are ultimately limited by gill surface area [6,7] (but see [8,9]).…”

Section: Introductionmentioning

confidence: 99%

Calcified gill filaments increase respiratory function in fishes

2020

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The morphology of fish gills is closely linked to aerobic capacity and tolerance of environmental stressors such as hypoxia. The importance of gill surface area is well studied, but little is known about how the mechanical properties of gill tissues determine function. In some fishes, the bases of the gill filaments are surrounded by a calcified ‘sheath' of unknown function. We tested two non-exclusive hypotheses: (i) calcified gill filaments enhance water flow through the gill basket, improving aquatic respiratory function, and (ii) in amphibious fishes, calcification provides support for gills out of water. In a survey of more than 100 species of killifishes and related orders, we found filament calcification was widespread and thus probably arose before the evolution of amphibious lifestyles in killifishes. Calcification also did not differ between amphibious and fully aquatic species, but terrestrial acclimation caused calcium deposition on the filaments of the killifish Kryptolebias marmoratus , suggesting a possible structural role when out of water. We found strong evidence supporting a role for filament calcification in enhancing aquatic respiratory function. First, acclimation to increased respiratory demands (hypoxia, elevated temperatures) induced calcium deposition on the filaments of K. marmoratus . Next, gentle removal of filament calcification decreased branchial resistance to water flow, indicating disruption of gill basket positioning. Thus, the mechanical properties of the gill filaments appear to play an important and previously unappreciated role in determining fish respiratory function.

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Interspecific and environment-induced variation in hypoxia tolerance in sunfish

Cited by 27 publications

References 84 publications

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

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

Oxidative cost of interspecific hybridization: a case study of two Triturus species and their hybrids

Calcified gill filaments increase respiratory function in fishes

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