Metabolic enzyme activities in shallow- and deep-water chondrichthyans: implications for metabolic and locomotor capacity

Condon, Nicole E.; Friedman, Jason R.; Drazen, Jeffrey C.

doi:10.1007/s00227-012-1960-3

Cited by 15 publications

(17 citation statements)

References 73 publications

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“…Contrary to this general hypothesis, enzymatic indices of white muscle glycolytic capacity suggest similar depth-related declines in metabolism between chondrichthyans and teleosts (Condon et al, 2012). However, the retention of aerobic capacity in muscles of chondrichthyans, but not teleosts, suggests a heavier reliance on costly endurance swimming, which could be inappropriate for an abyssal existence.…”

Section: Metabolic and Locomotory Constraintsmentioning

confidence: 69%

“…In white muscle of teleosts, the activities of enzymes related to glycolytic capacity decrease in correlation with the depth-related decline in whole-animal oxygen consumption rate . Glycolytic enzyme activities also decrease with depth in white muscle of chondrichthyans, implying similarly low metabolic rates as deep-sea teleosts (Condon et al, 2012;Drazen and Seibel, 2007;Treberg et al, 2003). By contrast, the aerobic enzyme activities in both types of muscles decline with depth in teleosts but not in chondrichthyans (Condon et al, 2012;Dickson et al, 1993;Drazen et al, 2013;Drazen and Seibel, 2007;SpeersRoesch et al, 2006;Treberg et al, 2003).…”

Section: Muscle Enzymes As a Proxy For Metabolic Ratementioning

confidence: 99%

“…Glycolytic enzyme activities also decrease with depth in white muscle of chondrichthyans, implying similarly low metabolic rates as deep-sea teleosts (Condon et al, 2012;Drazen and Seibel, 2007;Treberg et al, 2003). By contrast, the aerobic enzyme activities in both types of muscles decline with depth in teleosts but not in chondrichthyans (Condon et al, 2012;Dickson et al, 1993;Drazen et al, 2013;Drazen and Seibel, 2007;SpeersRoesch et al, 2006;Treberg et al, 2003). Other red muscle aerobic/oxidative properties are comparable between deep-sea and shallow demersal chondrichthyans (Bernal et al, 2003 The deep sea can be broadly defined as depths >200 m, incorporating the midwater (200-1000 m), bathyal (1000-4000 m), abyssal (>4000 m) and hadal (trenches >6000 m) zones.…”

Section: Muscle Enzymes As a Proxy For Metabolic Ratementioning

confidence: 99%

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Does the physiology of chondrichthyan fishes constrain their distribution in the deep sea?

Treberg

Speers‐Roesch

2016

Journal of Experimental Biology

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The deep sea is the largest ecosystem on Earth but organisms living there must contend with high pressure, low temperature, darkness and scarce food. Chondrichthyan fishes (sharks and their relatives) are important consumers in most marine ecosystems but are uncommon deeper than 3000 m and exceedingly rare, or quite possibly absent, from the vast abyss (depths >4000 m). By contrast, teleost (bony) fishes are commonly found to depths of ∼8400 m. Why chondrichthyans are scarce at abyssal depths is a major biogeographical puzzle. Here, after outlining the depth-related physiological trends among chondrichthyans, we discuss several existing and new hypotheses that implicate unique physiological and biochemical characteristics of chondrichthyans as potential constraints on their depth distribution. We highlight three major, and not mutually exclusive, working hypotheses: (1) the urea-based osmoregulatory strategy of chondrichthyans might conflict with the interactive effects of low temperature and high pressure on protein and membrane function at great depth; (2) the reliance on lipid accumulation for buoyancy in chondrichthyans has a unique energetic cost, which might increasingly limit growth and reproductive output as food availability decreases with depth; (3) their osmoregulatory strategy may make chondrichthyans unusually nitrogen limited, a potential liability in the food-poor abyss. These hypotheses acting in concert could help to explain the scarcity of chondrichthyans at great depths: the mechanisms of the first hypothesis may place an absolute, pressure-related depth limit on physiological function, while the mechanisms of the second and third hypotheses may limit depth distribution by constraining performance in the oligotrophic abyss, in ways that preclude the establishment of viable populations or lead to competitive exclusion by teleosts.

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Section: Metabolic and Locomotory Constraintsmentioning

confidence: 69%

Section: Muscle Enzymes As a Proxy For Metabolic Ratementioning

confidence: 99%

Section: Muscle Enzymes As a Proxy For Metabolic Ratementioning

confidence: 99%

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Does the physiology of chondrichthyan fishes constrain their distribution in the deep sea?

Treberg

Speers‐Roesch

2016

Journal of Experimental Biology

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“…Samples were homogenized in a 10:1 dilution using an ice cold titrated tris-buffer solution (pH of 7.55 at 10.0uC) with a motorized ground glass tissue homogenizer. CS was run first and without centrifuging the homogenate, as significant loss of activity (, 30% reduction) was observed for spun samples (Condon et al 2012). Subsequently, the homogenate was centrifuged (50,000 m s 22 for 5 min) prior to analysis of PK, LDH, and MDH.…”

Section: Methodsmentioning

confidence: 99%

Gill surface area and metabolic enzyme activities of demersal fishes associated with the oxygen minimum zone off California

Friedman

Condon

Drazen

2012

Limnology & Oceanography

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Metabolic enzyme activities and gill surface areas were measured across 10 species of demersal fishes from Monterey Canyon, California, which features a prominent oxygen minimum zone (OMZ). Comparisons were made between species living both within and outside of the OMZ. Enzyme activities showed no significant trend toward aerobic suppression or heightened reliance on anaerobic metabolism in response to the OMZ. While flatfish species living both within and outside of the OMZ had similarly low enzyme activities, the OMZ-dwelling Microstomus pacificus had 1.8-3 times larger gill surface area than comparably sized flatfishes from higher-oxygen waters, suggesting a morphological adaptation to low oxygen. In scorpaeniform fishes, high aerobic metabolism was accompanied by large gill surface areas in two routine-swimming OMZ-dwelling species (Anoplopoma fimbria and Careproctus melanurus). Low aerobic activities and small gills were found in two Sebastolobus species, suggesting a low oxygen demand resulting from a more sedentary behavior compared to other Scorpaeniformes. In gadiform fishes, no differences were measured in enzyme activity levels, but larger gill surface areas were measured in OMZdwelling Nezumia liolepis. These results indicate adaptation to low oxygen in a variety of ways that balance oxygen demand with supply, with no indication that these species rely on enhanced anaerobic metabolism. With both flatfishes and rattails, adaptation to OMZs is demonstrated through increased gill surface area.Oxygen minimum zones (OMZs) are midwater regions (200-1000 m) where dissolved oxygen levels are reduced by an order of magnitude relative to waters above and below the OMZ core, defined by a concentration of . 0.5 mL O 2 L 21 seawater (Levin 2003). While anoxic and hypoxic conditions exist temporarily in coastal margins, OMZs differ because they are temporally stable and impinge onto the continental shelf and slope.Recent data have indicated an ongoing expansion in several OMZs. Tropical OMZs have been simultaneously shoaling and deepening tens of meters over the past four decades (Stramma et al. 2010). Alaskan Gyre hypoxic waters (60 mmol L 21 ) have shoaled from 400 m to 300 m within the last five decades (Whitney et al. 2007). Additionally, California Current system dissolved oxygen levels have dropped, with the hypoxic boundary shifting 90 m vertically in the last three decades (Bograd et al. 2008).Given these recent expansions, there is a heightened importance in understanding how species living both within and nearby OMZs are adapted to low oxygen. Some benthic and midwater taxa associated with OMZ cores have been studied and exhibit adaptations to aerobically meet requirements for routine metabolism in low oxygen (Childress and Seibel 1998). However, little information is available to characterize how demersal fish species may react to changes in ambient oxygen concentrations.Fishes can cope with persistently low oxygen through two theoretical mechanisms that are not mutually exclusive: increased oxy...

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“…A number of enzymes have been utilized but most often the glycolytic enzymes, pyruvate kinase (PK) and lactate dehydrogenase (LDH), and the tricarboxylic acid (TCA) cycle enzymes, malate dehydrogenase (MDH) and citrate synthase (CS), are assayed because they generate ATP for muscle contraction and have correlated with whole‐body metabolic rate (Childress & Somero, ; Torres & Somero, ). Activities of these enzymes in white muscle (but not in brain or heart) decline with depth of occurrence in deep‐sea teleosts (Childress & Somero, ; Sullivan & Somero, ; Drazen & Seibel, ) and elasmobranchs (Treberg et al ., ; Condon et al ., ) generally corroborating respirometry measurements. It is thought that metabolism declines because increasing darkness reduces the distances over which predators and prey react to each other thus relaxing the selective pressure for high‐speed locomotory abilities and associated metabolic capacity (Seibel & Drazen, ).…”

Section: Introductionmentioning

confidence: 99%

Red muscle proportions and enzyme activities in deep‐sea demersal fishes

Drazen

Dugan

Friedman

2013

Journal of Fish Biology

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Owing to the paucity of data on the red muscle of deep-sea fishes, the goal of this study was to determine the proportions of red muscle in demersal fishes and its enzymatic activities to characterize how routine swimming abilities change with depths of occurrence. Cross sectional analysis of the trunk musculature was used to evaluate the proportion of red muscle in 38 species of Californian demersal fishes living at depths between 100 and 3000 m. The activity of metabolic enzymes was also assayed in a sub-set of 18 species. Benthic fishes had lower proportions of red muscle and lower metabolic enzyme activities than benthopelagic species. Mean proportion of red muscle declined significantly with depth with the greatest range of values in shallow waters and species with low proportions found at all depths. This suggested that while sedentary species occur at all depths, the most active species occur in shallow waters. Citrate synthase activity declined significantly with depth across all species, indicating that the mass-specific metabolic capacity of red muscle is lower in deep-sea species. These patterns may be explained by coupling of red and white muscle physiologies, a decrease in physical energy of the environment with depth or by the prevalence of anguilliform body forms and swimming modes in deep-living species.

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Metabolic enzyme activities in shallow- and deep-water chondrichthyans: implications for metabolic and locomotor capacity

Cited by 15 publications

References 73 publications

Does the physiology of chondrichthyan fishes constrain their distribution in the deep sea?

Does the physiology of chondrichthyan fishes constrain their distribution in the deep sea?

Gill surface area and metabolic enzyme activities of demersal fishes associated with the oxygen minimum zone off California

Red muscle proportions and enzyme activities in deep‐sea demersal fishes

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