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Coordination between ventilatory pressure oscillations and venous return in the cephalopod Sepia officinalis under control conditions, spontaneous exercise and recovery

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Abstract

Venous blood flow was measured for the first time in a cephalopod. Blood velocity was determined in the anterior vena cava (AVC) of cuttlefish S. officinalis with a Doppler, while simultaneously, ventilatory pressure oscillations were recorded in the mantle cavity. In addition, magnetic resonance imaging (MRI) was employed to investigate pulsatile flow in other major vessels. Blood pulses in the AVC are obligatorily coupled to ventilatory pressure pulses, both in frequency and phase. AVC peak blood velocity (vAVC) in animals of 232 (± 30 SD) g wet mass at 15°C was found to be 14.2 (± 7.1) cm s−1, AVC stroke volume (SVAVC) was 0.2 (± 0.1) ml stroke−1, AVC minute volume (MVAVC) amounted to 5.5 (± 2.8) ml min−1. Intense exercise bouts of 1–2 min resulted in 2.2-fold increases in MVAVC, enabled by 1.6-fold increments in both, AVC pulse frequency (f AVC) and vAVC. As increases in blood flow occurred delayed in time by 1.7 min with regard to exercise periods, we concluded that it is not direct mantle cavity pressure conveyance that drives venous return in this cephalopod blood vessel. However, during jetting at high pressure amplitude (> 1 kPa), AVC blood flow and mantle cavity pressure pulse shapes completely overlap, suggesting that under these conditions, blood transport must be driven passively by mantle cavity pressure. MRI measurements at 15°C also revealed that under resting conditions, f AVC and ventilation frequency (f V) match at 31.6 (± 2.1) strokes min−1. In addition, rates of pulsations in the cephalic artery and in afferent branchial vessels did not significantly differ from f AVC and f V. It is suggested that these adaptations are beneficial for high rates of oxygen extraction observed in S. officinalis and the energy conserving mode of life of the cuttlefish ecotype in general.

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Acknowledgments

This study was carried out in support of the project: The cellular basis of standard and active metabolic rate in the free-ranging cephalopod, Sepia officinalis (NER/A/S/2002/00812). The authors wish to thank Timo Hirse and Rolf Wittig for excellent technical support, Raymond and Marie-Paule Chichery (Université de Caen) for providing cuttlefish eggs in 2002 and 2003 and all student helpers that were engaged in raising the animals in our lab. Special thanks to Alison King for helpful and stimulating discussions on the subject of venous return in cephalopod and to two anonymous reviewers whose excellent criticism improved the manuscript.

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  1. Alfred Wegener Institut for Marine and Polar Research, Am Handelshafen 12, Bremerhaven, 27570, Germany

    Frank Melzner, Christian Bock & Hans-O. Pörtner

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  1. Frank Melzner
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  2. Christian Bock
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  3. Hans-O. Pörtner
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Correspondence to Frank Melzner.

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Communicated by G. Heldmaier

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Melzner, F., Bock, C. & Pörtner, HO. Coordination between ventilatory pressure oscillations and venous return in the cephalopod Sepia officinalis under control conditions, spontaneous exercise and recovery. J Comp Physiol B 177, 1–17 (2007). https://doi.org/10.1007/s00360-006-0104-9

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  • DOI: https://doi.org/10.1007/s00360-006-0104-9

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