Breathing pattern, CO2 elimination and the absence of exhaled NO in freely diving Weddell seals
Introduction
The extreme diving capabilities of Weddell seals (Leptonychotes weddelli) are due to their high storage capacity for oxygen (Qvist et al., 1986, Guyton et al., 1995, Kooyman and Ponganis, 1998) and its remarkably economical utilization mediated by the diving response (Scholander, 1940, Butler and Jones, 1997). In addition the management of pulmonary gas is paramount for efficient foraging in these animals. They exhale before and immediately after the dive, characteristics of their breathing pattern are obviously important for the handling of the considerable amount of pulmonary nitrogen as well as the regulation of buoyancy. So far only very few quantitative studies on the pattern of respiration before and the restoration of lung volume after free dives have been performed (Kooyman et al., 1971, Kooyman et al., 1973, Parkos and Wahrenbrock, 1987). As originally suggested by Scholander (1940) and in line with Kooyman et al. (1972) study in restrained seals, we have previously demonstrated indirect evidence (by determining blood nitrogen tensions) that the lungs of freely diving Weddell seals undergo alveolar collapse during descent between 25 and 50 m, a phenomenon stopping pulmonary gas exchange and, thus protecting these animals from the unwanted effects of excess nitrogen absorption (Falke et al., 1985). However, directly measured data on the mechanical events associated with lung compression, decompression and full recruitment at surfacing after each dive have been extremely scanty. In a freely diving trained dolphin, visible deformation of the chest wall began to occur between 10 and 60 m depth, and a photograph taken at 300 m depth showed marked thoracic compression from just behind the flippers and posteriorly (Ridgway et al., 1969). Following up on a suggestion of the late Professor Hermann Rahn (personal communication), we attempted to correlate the changes in lung volume during diving with measurements of thoracic circumference.
The aerobic diving limit (ADL) of Weddell seals is sufficient (15–20 min) for them to perform most underwater activities under aerobic metabolic conditions (Kooyman et al., 1983, Qvist et al., 1986, Castellini et al., 1992, Ponganis et al., 1993). In prolonged dives, however, the arterial blood oxygen tension () may fall below 20 mmHg (Qvist et al., 1986) suggesting that low is not necessarily the primary respiratory drive or the most important factor in the regulation of diving behavior (Stephenson, 2005). Instead, a profound impact of CO2 on respiration and diving (Pasche, 1976, Parkos and Wahrenbrock, 1987) has been reported but CO2 elimination was not quantified.
In humans, breath-holding causes a pronounced increase of gaseous nitric oxide concentrations in the upper respiratory tract (Gustafsson et al., 1991, Persson et al., 1990). By analogy we hypothesized that after the prolonged apnea of diving Weddell seals may also accumulate NO in the airways, and because of its potent selective pulmonary vasodilatory effects (Frostell et al., 1991) it might contribute to the re-establishment of pulmonary perfusion after recruitment of the lungs at surfacing.
In the present study, we aimed to extend previous observations (Kooyman et al., 1971, Kooyman et al., 1972, Kooyman et al., 1973, Kooyman, 1981b, Parkos and Wahrenbrock, 1987, Falke et al., 1985, Qvist et al., 1986) on the respiratory functions of freely diving Weddell seals firstly focusing on the respiratory pattern using measurements of respiratory flows as well as lung volumes and its shifts between dives. We quantified the changes in lung volume before, after and between dives expecting that the seal would decrease its lung volume significantly before and restore it to a large extent during the first few breaths after surfacing. We also expected that lung collapse during descent, and recruitment during ascent, would be associated with distinct corresponding changes in thoracic circumference, a hypothesis based on the above mentioned observation made in a dolphin by Ridgeway in 1969. Secondly we measured exhaled CO2 and hypothesized that post dive CO2 elimination () should correlate with the duration of the dive, a phenomenon which to our knowledge has not been previously reported in unrestrained Weddell seals. Thirdly, we hypothesized that NO should be present in the expired gas of seals in particular after the long breath-hold associated with long dives. Thus, we aimed to determine the concentration of endogenous NO in exhaled respiratory gas upon resurfacing.
Due to the constraints of our permit and due to the specific Antarctic environmental conditions our studies were restricted to three animals, consequently, our results are presented individually. These data were extremely difficult to obtain, hence, they should be considered a pilot study and hopefully will serve to stimulate future studies.
Section snippets
Animal handling and instrumentation
All seal studies were conducted under US NMFS marine mammal permit #600, and approved by the Massachusetts General Hospital Subcommittee on Research Animal Care. The general experimental procedure has been well described (Kooyman et al., 1971, Kooyman et al., 1973, Falke et al., 1985, Qvist et al., 1986, Parkos and Wahrenbrock, 1987). Five sub-adult male Weddell seals with weights estimated from 280 to 340 kg were captured near the Dellbridge Islands, the Erebus Glacier Tongue, and Arrival
Biometric data
We captured 5 Weddell seals (A–E), but physiological data could only be obtained from 3 seals C–E. Presented in Table 1 are their body weights (estimated according to Castellini and Kooyman, 1990).3 Because application of the strain gauge was a new technique we obtained reliable thoracic circumference measurements only in 2 seals (D and E).
Pattern of ventilation
We collected
Respiratory pattern and volumes
As a modification of the ingenious setup for pulmonary functions studies in freely diving Weddell seals developed by Kooyman et al., 1971, Kooyman et al., 1973, in which ventilation parameters were determined using classical spirometers and collecting bags, we employed a pneumotachograph to allow breath-by-breath measurement of respiratory flow rates and derived tidal volume by electrical signal integration. Resting values for breaths per minute, tidal and minute volumes as well as lung volumes
Acknowledgements
These studies were funded by National Science Foundation grant OPP 91-18192 and also supported by the Deutsche Forschungsgemeinschaft, grant DFG Fa 139/4. We thank Bernhard Huettel, the German representative of ECO Physics (Duernten, Switzerland) who provided the equipment for the NO measurements and Axel Mohnhaupt who provided the computer software. Special thanks goes to Professor Peter Scheid for his very valuable support in finalizing the manuscript.
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