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The thermal dependence of swimming and muscle physiology in temperate and Antarctic scallops

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DavidMarkBaileyPhDThesis.pdf (11.50Mb)
Date
2001
Author
Bailey, David Mark
Supervisor
Johnston, Ian A.
Peck, Lloyd
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Abstract
Swimming is important to the ecology of many species of scallop but the effects of temperature upon swimming are not clear. The ecology and natural history of scallops is introduced followed by a description of the state of current knowledge of scallop swimming, muscle physiology and energetics. The effects of temperature and the mechanisms used by ectotherms to compensate for such changes over acute, seasonal and evolutionary timescales are discussed. Scallops are active molluscs, able to escape from predators using jet propelled swimming. Queen scallops (Aequipecten opercularis) were acclimated to 5,10 and 15°C in the laboratory and collected in Autumn (13±3°C) and Winter (8±2°C) in order to investigate seasonal acclimatisation. The first jetting cycle of escape responses in these animals was recorded using high-speed video (200-250fps). Whole-animal velocity and acceleration were determined while measurements of valve movement and jet area allowed the calculation of muscle shortening velocity, force and power output. Peak swimming speed was significantly higher at 15°C (0.37m.s⁻¹) than at 5°C (0.28m.s⁻¹). Peak acceleration was 77% higher at 15°C (7.88m.s⁻²) than at 5°C (4.44m.s⁻²). Mean cyclic power output was also higher at 15°C (31.3W.kg⁻¹) than at 5°C (23.3W.kg⁻¹). Seasonal comparison of swimming in freshly caught animals revealed significantly greater acceleration (x2 at 11°C) and velocity during jetting in Winter than in Autumn animals (ANCOVA). These were associated with significant increases in peak power output (x8 at 11 °C), force production and muscle shortening velocity. Actomyosin ATPase activity was significantly higher (31 % at 15°C) in winter animals with peptide mapping of the Myosin heavy chain showing no differences between groups. Increases in muscle power output were associated with reductions in the length of the jetting phase as a proportion of the overall cycle. As a result large changes in muscle performance resulted in large short-term whole body performance enhancement but little difference to velocity over the cycle. Measurements of the swimming performance of the Antarctic scallop were made from videos of escape responses. Animals were acclimated to +2 and -1 °C in the laboratory and compared to animals maintained at natural water temperature (0±0.5°C) at the time of experimentation. Adamussium was very sensitive to temperature change with the proportion of swimming responses being less common at higher temperatures and where an individual was exposed to temperatures above it's maintenance temperature. Analysis of the first jetting cycle of swimming was carried out as described in Chapter 2. These analyses revealed that over the small temperature range that the animals can tolerate swimming performance is strongly temperature dependent. Q₁₀s above 2 included those for thrust (3.74), mean cyclic swimming speed (2.46), mean cyclic power output (5.71) and mean muscle fibre shortening velocity (2.16). Adamussium did not demonstrate strong phenotypic plasticity with no significant differences in swimming of muscle performance between animals acclimated to different temperatures. Comparison of the relationship between swimming velocity and temperature in Adamussium and other species showed little evidence for evolutionary compensation for temperature with all data fitting to a single relationship with a Q₁₀ of 1.96 (0-20°C). Similar results were obtained for power output and the performance of in vitro muscle preparations. These results are discussed in the light of field studies revealing the low predator pressure and escape performance of wild Adamussium. In vivo ³¹P-Nuclear Magnetic Resonance Spectrometry (MRS) was used to measure the levels of ATP, Phospho-l-arginine (PLA) and inorganic phosphorous (PI) in the adductor muscle of the Antarctic scallop, Adamussium colbecki, and two temperate species, Aequipecten opercularis and Pecten maximus. Graded exercise regimes from light (1-2 contractions) to exhausting (failing to respond to further stimulation) were imposed upon animals of each species. MRS allowed non-invasive measurement of metabolite levels and intracellular pH at high time resolution (30-120s intervals) during exercise and throughout the prolonged recovery period. Significant differences were shown between the magnitude and form of the metabolic response with increasing levels of exercise. Short-term (first 15 minutes) muscle alkalosis was followed by acidosis of up to 0.2 pH units during the recovery process. Aequipecten had significantly higher resting muscle PLA levels than either Pecten or Adamussium, used a five-fold greater proportion of this store per contraction and was able to perform only half as many claps (maximum of 24) as the other species before exhaustion. All species regenerated their PLA store at a similar rate despite widely different environmental temperatures. The major results and their impact on our knowledge of biomechanics and it's temperature dependence are discussed. Suggestions for future research based upon the experimental findings and techniques developed are presented.
Type
Thesis, PhD Doctor of Philosophy
Collections
  • Biology Theses
URI
http://hdl.handle.net/10023/7100

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