Physiological control of diving behaviour in the Weddell sealLeptonychotes weddelli: a model based on cardiorespiratory control theory

Abstract

Despite being obligate air breathers, many species of marine mammal are capable of spending most of their lives submerged in water. How they do this has been a subject of intense interest to physiologists for over a century, yet we still do not have a detailed understanding of the physiological mechanisms underlying this behaviour. What are the proximate mechanisms that trigger the 'decisions' to submerge and return to the surface? The present study proposes a model intended to address this question, based on fundamental concepts of cardiorespiratory control. Two basic hypotheses are examined by computer simulation, using a mathematical model of the mammalian cardiorespiratory control system with parameter values for an adult Weddell seal: (1) that the control of diving can be considered to be a respiratory control problem, and (2) that dives are initiated and maintained by disfacilitation of respiratory drive, not inhibition. Computer simulations confirmed the plausibility of these hypotheses. Simulated diving behaviour and physiological responses (ventilation, cardiac output, blood and tissue gas tensions) were consistent with published data from freely diving Weddell seals. Dives up to the estimated aerobic dive limit (ADL, 18-25·min) could be simulated without the need for active inhibition of breathing in this model. This theoretical analysis suggests that the most important physiological adjustments occur during the surface interval phase of the dive cycle and include hyperventilation accompanied by high cardiac output, appropriate regulation of cerebral blood flow and central chemoreceptor threshold shifts. During dives, cardiac output, distribution of peripheral blood flow, splenic contraction and peripheral chemoreflex drives were found to modulate physiological and behavioural responses, but were not essential for simulated dives to occur. The main conclusion from this study is that the central chemoreceptor may be an important mechanism involved in the regulation of diving behaviour, implying that CO 2 , not O 2 , is the key regulatory variable in this model. This model includes and extends the ADL concept and suggests an explicit mechanism by which the respiratory control system may play a central role in the regulation of diving behaviour. It is likely that respiratory mechanisms are an important component of a hierarchical behavioural control system and further studies are required to test the qualitative and quantitative validity of the model.

A Phylogenetic Analysis of the Allometry of Diving

“…Moreover, some species of birds, at least, remove CO 2 in excess of the rate at which it is produced just before submerging, probably to ensure that high levels of CO 2 during submersion do not produce an urge to surface and breathe while there are still sufficient oxygen stores remaining (Halsey et al 2003a). A similar phenomenon has been proposed for Weddell seals (Stephenson 2005). In addition, birds in particular may spend varying periods of time at the surface engaged in other activities, such as preening.…”

Blood oxygen depletion during rest-associated apneas of northern elephant seals (Mirounga angustirostris)

“…End-of-apnea P CO 2 showed an increasing trend as apnea duration increased, varying between 49 and 70·mmHg, while pH fluctuated by less than 0.1 pH unit. In previous studies (Milsom et al, 1996;Stephenson, 2005), it has been suggested that CO 2 may play a primary role in the drive to breathe, but such investigations of respiratory control were beyond the scope of the present project. Our results serve only to demonstrate that end-of-apnea levels are variable in the blood and that there is no apparent threshold associated with the end of apnea.…”

Myoglobin's old and new clothes: from molecular structure to function in living cells

“…Oxidative metabolism during apnea, however, poses a challenge for CO 2 disposal. Excess CO 2 can alter respiratory drive as well as sleep structure (Milsom et al, 1996;Skinner and Milsom, 2004;Stephenson, 2005). Even though marine and terrestrial mammals have a similar hypercarbic chemosensitivity, the higher blood buffering capacity allows marine mammals to accommodate the CO 2 build-up…”