Metabolic rate, respiratory partitioning and the implications for dive duration in the bimodally respiring Arafura filesnake, Acrochordus arafurae

Kirstin Pratt (2009). Metabolic rate, respiratory partitioning and the implications for dive duration in the bimodally respiring Arafura filesnake, Acrochordus arafurae PhD Thesis, School of Biological Sciences, The University of Queensland.

       
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Author Kirstin Pratt
Thesis Title Metabolic rate, respiratory partitioning and the implications for dive duration in the bimodally respiring Arafura filesnake, Acrochordus arafurae
School, Centre or Institute School of Biological Sciences
Institution The University of Queensland
Publication date 2009-07
Thesis type PhD Thesis
Supervisor Craig Franklin
Robbie Wilson
Total pages 127
Total colour pages 1
Total black and white pages 126
Subjects 06 Biological Sciences
Abstract/Summary Diving vertebrates are constrained by an aquatic existence because they carry a limited store of oxygen whilst submerged and must return to the surface to breathe. Therefore, oxygen stores must be used efficiently in order to maximise aerobic dive duration. The ability to use additional, non-pulmonary gas exchange to obtain oxygen from the water provides a mechanism to alleviate the use of body oxygen stores and extend dive duration. The partitioning of gas exchange between aerial and aquatic modes is predicted by the theory of optimal breathing. As the cost of obtaining oxygen by one mode increases, the reliance on this mode should decrease whilst the reliance on the alternate mode should increase. A number of environmental, physiological and ecological factors can affect metabolic rate and/or the partitioning of gas exchange between aerial and aquatic modes, with consequences for dive duration. The overall aim of this study was to examine the effects of temperature, specific dynamic action and predation on respiratory partitioning and diving behaviour in the Arafura filesnake, Acrochordus arafurae. Filesnakes provide an excellent model to address the aims of this study because they are fully-aquatic and respire bimodally, utilising both aerial and aquatic (cutaneous) gas exchange. Metabolic rate and diving behaviour are usually thermally dependent in diving ectotherms. Given this knowledge, we tested whether A. arafurae was capable of up-regulating cutaneous oxygen uptake to compensate for the temperature induced increases in metabolic rate. Metabolic rate had a Q10(20-32°C) of 2.33, however cutaneous oxygen uptake was independent of temperature and all elevated metabolic demands were met by increasing aerial oxygen uptake. Consequently, maximum dive duration was reduced by 70%, from 77 min at 20°C to 28 min at 32°C. The temperature independence of cutaneous oxygen uptake suggests that blood PO2 remained stable across temperatures and the increased blood flow expected with an elevated metabolic rate did not enhance the capacity for oxygen uptake (diffusion limited rather than perfusion limited). Although cutaneous oxygen uptake was not regulated, its contribution to extending dive duration was significant. When the ability to respire aquatically was removed (severe hypoxia), dive duration was reduced by up to 30%. Acrochordus arafurae feeds infrequently on large, high-protein meals thus the postprandial metabolic response was significant. Meal size and fast length (13 days or one month) were both positively related to the peak metabolic scope. After fasting for one month, peak rate of oxygen consumption was up to 12-fold standard metabolic rate (SMR) with the largest meal size. By comparison, an animal that was fasted for 13 days and fed an equivalent meal size incurred a six-fold increase in SMR. The energetic costs of digestion (specific dynamic action, SDA) increased with meal size, but fast length had no effect, suggesting the up-regulation of gut function was not a significant cost in the SDA. Pulmonary and cutaneous gas exchange increased with elevated metabolic demands however pulmonary oxygen uptake was the dominant mode. Despite the increase in cutaneous oxygen uptake during digestion, maximum dive duration decreased by between 50% and 90% of fasted values. The significant reductions in dive duration following feeding may have implications for predator vulnerability. Diving animals are most vulnerable to predation at the water’s surface. The theory of optimal diving under predation predicts that animals should make shorter, more frequent surface intervals or longer, less frequent surfacing intervals to minimise exposure to predators. Acrochordus arafurae is prone to aerial (birds of prey) and aquatic (crocodiles, large fish) predation. Simulated avian predation did not change dive or surface duration or proportion of time at the surface or spent active. However, a greater number of longer dives were observed with fewer long surface intervals suggesting an increase in the use of cutaneous oxygen uptake. The nocturnal diving patterns of A. arafurae provide an in-built anti-predator strategy. The threat of aquatic predation by a large fish produced atypical anti-predator responses; A. arafurae became increasingly active, reduced dive duration and increased surface interval which was indicative of a foraging response. The field diving behaviour of adult A. arafurae was determined using acoustic telemetry and interpreted in the context of environmental and ecological conditions. The mean dive duration was 6.6 min, with 85% of dives less than 10 min in duration. The maximum dive duration was 153 min. There was no diel pattern in dive duration. Snakes were located at an mean depth of 0.62 m, however, they occasionally ventured to greater depths (up to 6 m) but very infrequently. Snake body temperature reflected water temperature and fluctuated by approximately 1°C on a daily basis. The short and shallow dives of A. arafurae minimise travel costs associated with surfacing and may be an anti-predator strategy. Metabolic rate and respiratory partitioning is dependent on physiological and ecological factors with consequences for dive duration. Temperature and postprandial induced increases in metabolic demands were met by increasing the reliance on aerial gas exchange given the limitations of cutaneous gas exchange; and dive duration was substantially reduced as a result. Ecological factors, such as predation, can increase the cost of surfacing and promote the use of aquatic gas exchange. However, changes to behaviour, including habitat choice, residence depth and the employment of a diving strategy that does not maximise dive duration may be just as effective at minimising the costs and maximising the gains of a dive.
Keyword Acrochordus
bimodal gas exchange
digestion
hypoxia
optimal diving
predation
rate of oxygen consumption
reptile
specific dynamic action
temperature
Additional Notes 25

 
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Created: Sat, 21 Nov 2009, 08:13:06 EST by Ms Kirstin Pratt on behalf of Library - Information Access Service