Thermal plasticity of skeletal muscle mitochondrial activity and whole animal respiration in a common intertidal triplefin fish, Forsterygion lapillum (Family: Tripterygiidae)

Javed Rafiq Khan, F. I. Iftikar, N. A. Herbert, Erich Gnaiger, A. J. R. Hickey

Research output: Contribution to journalJournal articleResearchpeer-review

Abstract

Oxygen demand generally increases in ectotherms as temperature rises in order to sustain oxidative phosphorylation by mitochondria. The thermal plasticity of ectotherm metabolism, such as that of fishes, dictates a species survival and is of importance to understand within an era of warming climates. Within this study the whole animal O-2 consumption rate of a common New Zealand intertidal triplefin fish, Forsterygion lapillum, was investigated at different acclimation temperatures (15, 18, 21, 24 or 25 A degrees C) as a commonly used indicator of metabolic performance. In addition, the mitochondria within permeabilised skeletal muscle fibres of fish acclimated to a moderate temperature (18 A degrees C Cool acclimation group-CA) and a warm temperature (24 A degrees C. Warm acclimation group-WA) were also tested at 18, 24 and 25 A degrees C in different states of coupling and with different substrates. These two levels of analysis were carried out to test whether any peak in whole animal metabolism reflected the respiratory performance of mitochondria from skeletal muscle representing the bulk of metabolic tissue. While standard metabolic rate (SMR- an indicator of total maintenance metabolism) and maximal metabolic rate (O-2 (max)) both generally increased with temperature, aerobic metabolic scope (AMS) was maximal at 24 A degrees C, giving the impression that whole animal (metabolic) performance was optimised at a surprisingly high temperature. Mitochondrial oxygen flux also increased with increasing assay temperature but WA fish showed a lowered response to temperature in high flux states, such as those of oxidative phosphorylation and in chemically uncoupled states of respiration. The thermal stability of mitochondria from WA fish was also noticeably greater than CA fish at 25 A degrees C. However, the predicted contribution of respirational flux to ATP synthesis remained the same in both groups and WA fish showed higher anaerobic activity as a result of high muscle lactate loads in both rested and exhausted states. CA fish had a comparably lower level of resting lactate and took 30 % longer to fatigue than WA fish. Despite some apparent acclimation capacity of skeletal muscle mitochondria, the ATP synthesis capacity of this species is constrained at high temperatures, and that a greater fraction of metabolism in skeletal muscle appears to be supported anaerobically at higher temperatures. The AMS peak at 24 A degrees C does not therefore represent utilisation efficiency of oxygen but, rather, the temperature where scope for oxygen flow is greatest.
Original languageEnglish
JournalJournal of Comparative Physiology B: Biochemical, Systems, and Environmental Physiology
Volume184
Issue number8
Pages (from-to)991-1001
ISSN0174-1578
DOIs
Publication statusPublished - 2014
Externally publishedYes

Keywords

  • PHYSIOLOGY
  • ZOOLOGY
  • AEROBIC SCOPE
  • SWIMMING PERFORMANCE
  • ONCORHYNCHUS-MYKISS
  • METABOLIC-RATE
  • RAINBOW-TROUT
  • TEMPERATURE
  • ACCLIMATION
  • CLIMATE
  • RESPIROMETRY
  • DEPENDENCE
  • Mitochondria
  • Temperature acclimation
  • Electron transport system
  • Lactate
  • Anerobic metabolism
  • Life Sciences
  • Animal Physiology
  • Biomedicine general
  • Human Physiology
  • Zoology
  • Biochemistry, general
  • Biomedical and Life Sciences
  • Physiology
  • Ecology, Evolution, Behavior and Systematics
  • Animal Science and Zoology
  • Biochemistry
  • Endocrinology
  • Medicine (all)
  • Animalia
  • Forsterygion lapillum
  • Pisces
  • Tripterygiidae
  • biological marker
  • lactic acid
  • acclimatization
  • analysis of variance
  • animal
  • biological model
  • blood
  • climate change
  • energy metabolism
  • mitochondrion
  • New Zealand
  • oxygen consumption
  • Perciformes
  • physiology
  • skeletal muscle
  • species difference
  • temperature
  • Acclimatization
  • Analysis of Variance
  • Animals
  • Biological Markers
  • Climate Change
  • Energy Metabolism
  • Lactic Acid
  • Models, Biological
  • Muscle, Skeletal
  • Oxygen Consumption
  • Species Specificity
  • Temperature
  • Biochemistry studies - General
  • Biochemistry studies - Nucleic acids, purines and pyrimidines
  • Physiology - General
  • Metabolism - General metabolism and metabolic pathways
  • Muscle - Physiology and biochemistry
  • lactate
  • oxygen
  • ATP
  • Animals, Chordates, Fish, Nonhuman Vertebrates, Vertebrates
  • respiration
  • acclimation temperature
  • standard metabolic rate
  • thermal plasticity
  • respiratory performance
  • aerobic metabolic scope
  • Biomarkers

Fingerprint Dive into the research topics of 'Thermal plasticity of skeletal muscle mitochondrial activity and whole animal respiration in a common intertidal triplefin fish, Forsterygion lapillum (Family: Tripterygiidae)'. Together they form a unique fingerprint.

Cite this