The effects of depth on the cardiac and behavioural responses of double-crested cormorants (Phalacrocorax auritus) during voluntary diving
Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia, Canada V6T 1Z4
*Present address: Centre dEcologie et Physiologie Energetiques, CNRS, 23 Rue Becquerel, 67087 Strasbourg Cedex 2, France (e-mail: manfred.enstipp{at}c-strasbourg.fr)
Accepted September 12, 2001
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: diving, double-crested cormorant, Phalacrocorax auritus, heart rate, behaviour, depth, carotid body chemoreceptor, blood gas, data logger, cardiac control mechanism.
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Intravascular chemoreceptors (carotid bodies) that monitor changes in O2 and CO2 levels and pH in the arterial blood have been shown to be important in the cardiac responses to diving in both forcedly and voluntarily diving ducks. In freely diving tufted ducks (Aythya fuligula), the carotid bodies perform a role in maintaining and reinforcing the initial decline in heart rate during the later part of shallow dives (Butler and Woakes, 1982a; Butler and Stephenson, 1988
), although a role for other receptors cannot be excluded, especially when dives are long (Butler and Stephenson, 1988
). Certainly, pressure changes during dives to depth will alter any chemoreceptor-driven response, while leaving the contribution from other receptors unaffected. During the descent phase of deep dives, overall pressure will increase by 1 atmosphere (101 kPa) for every 10 m of depth. This compression will increase alveolar oxygen tension (PAO2) and may augment blood oxygenation at depth (Lanphier and Rahn, 1963
). Markedly elevated arterial oxygen tensions (PaO2) during the early descent phase of deep dives have been found during simulated dives to depth in Adélie (Pygoscelis adeliae) and gentoo (P. papua) penguins, in freely diving Weddell seals (Leptonychotes weddelli) and in breath-hold dives to depth in humans (Kooyman et al., 1973
; Qvist et al., 1986
; Qvist et al., 1993
). This elevation in PaO2 might have consequences for the development of the cardiac response during deep diving because it would inhibit the contribution of the chemoreceptors and, hence, delay the reinforcement of any initial decline in heart rate. However, alveolar CO2 tension (PACO2) also increases during descent, so a higher PaCO2 might counteract the effects of a high PaO2.
Besides their effects on the cardiovascular performance of diving animals, blood gas levels are important regulators of ventilation. Adjustment of dive duration and the length of the subsequent surface interval are important behavioural components in the regulation of ventilation in diving animals. Hence, blood gas levels might play an important role in controlling dive behaviour, as has been shown for tufted ducks (Butler and Stephenson, 1988). The importance of blood gas levels in modulating the cardiac and behavioural responses to voluntary shallow and deep diving has never been investigated in cormorants. Forced submergence studies on double-crested cormorants revealed equivocal results. While Mangalam and Jones (1984
) found that breathing different levels of O2 and CO2 before forced submergence had little effect on the bradycardia displayed during submergence, Jones and Larigakis (1988
) reported significantly elevated heart rates during forced submergence after exposure to 100 % O2 before submersion.
Double-crested cormorants in British Columbia are opportunistic foragers, taking the majority of their prey in the littoral-benthic zone (Robertson, 1974). Although direct measurements of dive depth are not available, double-crested cormorants have been reported to dive in water ranging in depth from 1 to 20 m (Ross, 1974
; Ainley et al., 1990
; King et al., 1995
). If double-crested cormorants forage predominantly on benthic prey, the maximum dive duration of 70 s (Munro, 1927
) suggests that they are capable of submerging to even greater depths. Hence, double-crested cormorants are likely to experience the physiological effects of a substantial increase in ambient pressure during diving. The purpose of our study, therefore, was to investigate the effects of depth, especially as it affects blood gas levels, on cardiac and behavioural control during diving.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Training protocol
Within the first 3 months of capture, the cormorants were introduced into the shallow dive tank (9 m longx3 m widex1 m deep). The surface of the shallow dive tank was progressively covered during the training sessions until only a small section at one end of the tank remained open. Birds submerged here, swam to the opposite end of the tank where chopped herring pieces had been placed, picked up a piece of fish and returned to the uncovered section to swallow their prey (Fig. 1A) (shallow horizontal dives). A few weeks later, the birds were rotated between the shallow dive tank and the outdoor holding pens. Five of the nine cormorants were introduced into the deep dive tank (13 m highx5 m in diameter), where they were trained to pick up chopped herring pieces from a feeding platform suspended within the water column (12 m water depth) (Fig. 1B) (deep vertical dives). Starting 34 weeks before data collection, birds were captured on a daily basis, equipped with a harness holding a dummy data logger and placed onto the shallow or deep dive tank. After one complete foraging bout, the birds were recaptured for removal of the harness and returned to their pens. A foraging bout was defined as the time from a birds entrance into the water until it voluntarily stopped diving for at least 10 min. Water temperature in the tanks varied between approximately 6°C in winter and approximately 16°C in summer, which is close to the seasonal variation that would be experienced by wild double-crested cormorants on the south-west coast of British Columbia.
|
The birds were given at least 1 week to recover from surgery before the start of the experiments. Before a trial, a cormorant was caught in its holding pen, and the harness with data logger was placed on its back. The data loggers ECG electrode leads were connected to the implanted leads, and the sampling mode of the data logger was triggered. The handling time of the birds was kept to a minimum and usually did not exceed 5 min. The birds were immediately introduced into the shallow or deep dive tank, where they started diving spontaneously. To avoid disturbance, the trials were filmed using a video camera. At the end of a trial, which generally lasted 2030 min, the birds were recaptured to unplug the ECG leads and remove the harness. The birds were released into their holding pens, and the data were downloaded from the data logger into a personal computer.
Blood gas levels (O2 and CO2) were manipulated before the onset of a dive bout by exposing the birds to different gas mixtures. On both the shallow and deep dive tank, a transparent polyvinylchloride (PVC) cage (0.8 m longx0.6 m widex0.6 m high), covering the opening of the surface cover, was filled with the desired gas mixture from a gas bottle. The PVC cage was kept airtight by immersing its open bottom part; however, two small holes had to be introduced for a trapdoor that allowed some gas to escape. Gas samples were drawn continuously from the cage during the entire trial and analysed for their O2 and CO2 contents (Beckman O2-analyser OM11 and Beckman CO2-analyser LB-2; Beckman Instruments Inc., Schiller Park, IL, USA) to ensure that the desired mixture was maintained.
After the introduction of a bird into the cage, the gas flow was readjusted until the desired gas concentration stabilised. Water access was controlled through a trapdoor at the bottom of the cage. Birds were exposed to the stabilised gas mixture for 10 min before the trapdoor was opened and the dive bout started. During the trial, the gas flow into the cage was kept at a low but sufficient rate to keep the gas concentration stable. All birds were familiarised with the cage during training sessions. In the shallow dive tank, birds were exposed to the following gas mixtures: (i) normal air (control); (ii) hyperoxic air mixture (>80 % O2); (iii) hypoxic air mixture (12 % O2); (iv) hypercapnic/normoxic mixture (3 % CO2 and air); or (v) hypoxic/hypercapnic mixture (12 % O2 and 3 % CO2). Preliminary trials in the shallow dive tank showed that hypercapnia had little effect on the cardiac response during voluntary diving. Hence, the hypercapnic trials were discontinued, so these data are available for the shallow dive tank only. In the deep dive situation, birds were exposed to only normoxic (control) and hypoxic gas mixtures (here 89 % O2). The lower oxygen concentration for the hypoxic mixture in the deep dive situation was chosen because, in preliminary trials, the compression experienced by the birds during descent and the accompanying increase in PAO2, and therefore in PaO2, appeared to prevent the chemoreceptor response at the level of hypoxia chosen for the shallow dive situation (12 % O2).
All gas mixtures were administered at random. Although blood gas levels were not measured in this study, we are confident that the administration of the different gas mixtures used in this study for 10 min before diving produced the desired changes in blood gas levels. Mangalam and Jones (1984) elevated the PaO2 of double-crested cormorants almost threefold (from 80 to 220 mmHg; from 10.7 to 29.3 kPa) by administering 50 % O2 for 5 min prior to forced submergence. Breathing 12.8 % O2 reduced PaO2 to 70 mmHg (9.33 kPa).
Cormorants did not rest while on the water but dived continuously until leaving the water at the end of the foraging bout. Hence, resting heart rates were obtained from five birds while they were in their outdoor holding pens. Birds were equipped with the data logger and harness as described above but kept inside their holding pens. The birds perched immediately after release and returned to their routine shortly after the handler departed. Trials lasted for approximately 1 h and were carried out during daylight hours with post-absorptive birds that were awake and perched in an upright position.
Data analysis and statistics
To allow comparison between the different experimental situations and to reduce the influence of dive duration on the expression of the cardiac response to voluntary diving, only dives between 18 and 22 s in duration and only dives with an obvious foraging intention (i.e. birds swam to the feeding spot) were selected for analysis of heart rate. After training, the majority of dives by cormorants in the shallow and deep dive tanks fell into this category. Submergence and emergence times were determined from the record of the data loggers submergence sensor. Cardiac interbeat intervals were derived from the ECG trace after identifying the QRS peaks by eye. A mean value for the interbeat intervals of each dive was calculated and subsequently converted into heart rate (beats min1).
For each cormorant in each different treatment, six dives were analysed. A mean value for each bird was calculated from the six individual dives per treatment. For each treatment, a grand mean was calculated from the individual bird means. To compute heart rate profiles for the different experimental treatments, heart rate data were divided into 3 s intervals, starting 9 s before a dive and ending 9 s after its completion. Mean values for these intervals were calculated for all dives and used to generate grand means as described above. To investigate the effect of dive duration on the cardiac response during voluntary diving, all shallow dives performed by three individuals (dive duration 328 s) were included in a separate analysis.
To calculate resting heart rate, the instantaneous heart rate over the entire resting trial was plotted against time. Heart rate was elevated because of handling at the beginning of the trial but fell to a baseline value within 10 min. When heart rate had reached a stable level, a period of 20 min was chosen for the calculation of a single resting heart rate value. A mean value was calculated from all interbeat intervals during that selected period and converted into heart rate.
Dive behaviour was investigated by computing dive duration, surface interval duration and dive/pause ratios for five birds. For each cormorant in each different treatment (in both the shallow and deep dive tanks), ten dives and the subsequent surface intervals were selected at random from diving bouts in which birds performed at least three successive feeding dives. Only dives with a clear foraging intention (see above), lasting between 15 and 30 s and for which the subsequent surface interval did not mark the end of a dive bout were included in the analysis.
One-way repeated-measures analysis of variance (ANOVA) with StudentNewmanKeuls pairwise multiple comparisons was used for comparison among different treatments during shallow diving (air, hyperoxia, hypoxia, etc.) and among different phases of the dive (pre-dive, dive, post-dive). When single comparisons were made, as in comparing values obtained from the two treatments during deep diving (normoxia and hypoxia), Students paired t-test was used. Significance was accepted at P<0.05. The average relationship between mean dive heart rate and dive duration that takes into account variability between subjects was determined using repeated-measures multiple linear regression, with each cormorant being assigned a unique index variable. All mean values are presented with the standard deviation (± S.D.).
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
|
|
Cardiac responses to diving after breathing various gas mixtures
Manipulating the oxygen content of the inspired air before diving had marked effects on heart rate during diving (Fig. 5). Exposure to the hyperoxic gas mixture in the shallow dive tank increased the mean dive heart rate significantly (to 195.4±13.0 beats min1) compared with the normoxic control situation (174.3±13.4 beats min1). Upon submersion, heart rate initially fell to a similar level as in the control situation, but did not decline appreciably during the rest of the dive (Fig. 6). Exposure to the hypoxic gas mixture reduced the mean dive heart rate significantly in both the shallow (to 154.0±11.5 beats min1) and the deep (to 153.3±17.1 beats min1) dive situation compared with normoxic dives (Fig. 5). The course of the heart rate response during diving after hypoxic exposure was almost identical in both situations, and heart rate stayed well below the control level throughout the dives (Figs 6, 7). Also, hypoxia reduced pre- and post-dive heart rates, with a more pronounced reduction in the deep dive situation, where the level of hypoxia was more severe. Inspiration of elevated levels of CO2 before diving in the shallow dive tank had little effect on mean dive heart rate (Fig. 5) or the time course of the heart rate response. In the case of the hypercapnic hypoxic exposure, no further reduction in dive heart rate, beyond the response seen after hypoxic exposure alone, was detectable.
|
|
|
Dive behaviour
There was no significant difference in the mean dive duration of normoxic birds, whether diving in the shallow or the deep dive tank (20.43±0.83 s and 20.29±1.37 s respectively) (Fig. 8). The duration of the surface interval following a dive, however, was significantly different (shallow 9.08±1.45 s, deep 15.05±3.37 s), resulting in a higher dive/pause ratio during shallow diving (2.54±0.33 versus 1.48±0.38).
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The cardiac responses of double-crested cormorants during deep diving were comparable with the moderate heart rate changes displayed by diving ducks and Humboldt and Adélie penguins during shallow diving (Stephenson et al., 1986; Furilla and Jones, 1986, 1987
; Butler and Woakes, 1976
, 1979
, 1984
; Culik, 1992
). They were also similar to heart rates reported for two freely diving double-crested cormorants (Kanwisher et al., 1981
).
The greater cardiac response during shallow diving, compared with deep diving, closely resembled the response shown by tufted ducks making extended horizontal dives in a covered 2.8 m deep tank (Stephenson et al., 1986). In these dives, averaging 41.4 s, the heart rate of ducks declined steadily after approximately 7.5 s, reaching sub-resting levels after approximately 27.5 s. These tufted ducks, like our cormorants during shallow diving, had to swim actively towards and away from the feeding spot, while cormorants during vertical deep diving returned to the surface more or less passively. Hence, it is conceivable that the energetic costs of shallow horizontal dives might be increased, compared with deep, vertical dives. First, passive surfacing from deep vertical dives will reduce locomotor effort and save energy during these dives. Second, buoyancy during deep vertical diving will be reduced, compared with shallow horizontal diving, further decreasing energy expenditure (Lovvorn and Jones, 1994
). In lesser scaups (Aythya affinis) performing shallow (1.5 m) but vertical dives, buoyancy is the dominant factor determining dive costs (Stephenson, 1994
). Loss of air from the plumage layer and compression of the buoyant air spaces due to hydrostatic pressure decrease buoyancy at depth in these lesser scaups by 32 % compared with the surface (Stephenson, 1994
). Third, swimming close to the surface during shallow horizontal diving (as observed in our cormorants) will increase drag and add to the energetic cost of these dives (Hertel, 1969
). Hence, ducks and cormorants performing shallow horizontal dives face an energetically challenging situation. If oxygen is used up at a faster rate during shallow horizontal diving than during deep vertical diving, PaO2 would be depleted more rapidly and evoke a stronger cardiac response via intravascular chemoreceptors during these shallow dives.
The difference in the heart rate response to shallow and deep diving might be further accounted for by the effects of pressure changes associated with deep diving on the cardio-pulmonary system. Birds diving to depth will experience a compression hyperoxia during descent (Lanphier and Rahn, 1963; Kooyman et al., 1973
; Qvist et al., 1986
). If PaO2 stays elevated during this phase of the dive (Qvist et al., 1993
), any chemoreceptor-mediated reinforcement of the initial reduction in heart rate will be delayed as a consequence. Although the compression hyperoxia during descent will be accompanied by an increase in PaCO2, this seems to have little effect on the cardiac response expressed (see below). Energetic savings, due to the reduced locomotor effort during the bottom (reduced buoyancy at depth) and ascent (passive surfacing) phases of deep-diving cormorants, will help to maintain a relatively high PaO2, further delaying any chemoreceptor contribution to the cardiac response. Hence, heart rate stayed well above the resting level during these relatively short dives (1822 s). It is conceivable that in longer dives heart rate will fall more drastically, because PaO2 will drop, provoking a chemoreceptor-driven cardiac inhibition. In fact, marked cardiac responses were observed in much longer (range 140287 s) and deeper (range 35101 m) dives of South Georgian shags diving at sea (Bevan et al., 1997
). In these dives, heart rate fell to a level near the resting value in the early phase (after approximately 30 s) and reached sub-resting levels later in the dive. In contrast to this deep-diving scenario, shallow-diving birds will not experience a compression hyperoxia; hence, PaO2 will decrease early in the dive (especially if shallow horizontal diving is, in fact, associated with increased energetic costs), enhancing any chemoreceptor-mediated cardiac inhibition.
During the ascent phase of deep dives, PAO2 will fall rapidly (Lanphier and Rahn, 1963), potentially reversing the direction of oxygen transport (Olszowka and Rahn, 1987
). Accordingly, there should be a drop in PaO2, which would increase the chemoreceptor drive and, in turn, reduce heart rate. In the present study, however, heart rate did not decrease further during ascent and actually increased just before birds reached the surface. Obviously, other neurological inputs must override the chemoreceptor contribution during this phase of deep dives. In addition to possible influences of higher brain centres, anticipating the return to the surface, re-expansion of the respiratory system might activate pulmonary stretch receptors, which would in turn increase heart rate (Harrison, 1960
; Kooyman, 1989
). Increasing heart rate in anticipation of surfacing seems to be a usual feature of the cardiac response to voluntary diving in birds and mammals (Butler and Jones, 1997
). For ringed seals (Phoca hispida), it has been shown that visual orientation is important in facilitating the anticipatory increase in heart rate during ascent (Elsner et al., 1989
), which stresses the influence of components of the central nervous system above the reflex level.
In the only other laboratory study in which the heart rate of diving birds was recorded during dives of greatly varying depth (de Leeuw et al., 1998), tufted ducks showed no relationship between heart rate at different phases of the dive cycle and dive depth. Heart rate during diving was similar whether diving to 1.5 m (averaging 12.7 s) or to 5.5 m (averaging 26.5 s). In other words, compression hyperoxia did not seem to affect heart rate during diving. Since dive duration increased considerably with depth, however, this effect might have been masked by the effects of dive duration on heart rate. Descending to 5.5 m will take longer and, hence, will require more oxygen than descending to 1.5 m. As a consequence, the greater drop in PaO2 due to the longer time required to reach the bottom in deep dives might counteract the effects of an increased PaO2, due to compression hyperoxia, on heart rate.
Taken together, the following findings seem to suggest that intravascular chemoreceptors are important in mediating the cardiac responses during voluntary diving in double-crested cormorants. First, the secondary, more gradual, decline in heart rate observed a few seconds after initiation of a shallow dive (Fig. 2) might reflect an increase in chemoreceptor discharge frequency caused by a reduction in PaO2. Second, the significant linear relationship between mean dive heart rate and dive duration found for three birds during shallow diving (Fig. 4) suggests that a gradual mechanism facilitates the reduction in heart rate, again pointing at chemoreceptors. Third, in deep dives, during which PaO2 will be elevated initially as a result of hydrostatic compression, heart rate stayed relatively stable throughout the dive or declined at a much slower rate compared with shallow dives.
Alteration of inspired gas composition
The results obtained from experimental manipulation of the oxygen content in the inspired air before diving further emphasise the importance of intravascular chemoreceptors for cardiac control during voluntary diving in double-crested cormorants. Our findings are in agreement with results reported for voluntarily diving tufted and redhead (Aythya americana) ducks. In tufted ducks, chronic bilateral denervation of the carotid bodies had no effect on the immediate reduction in heart rate upon submersion (Butler and Woakes, 1982b). Heart rate was, however, significantly elevated towards the end of spontaneous dives. Similarly, Furilla and Jones (1986
) found that altering the level of O2 breathed by redhead ducks before voluntary submersion had no effect on heart rate early in the dive (after 25 s of submergence). Dive duration, however, was positively correlated with the level of oxygen in the inspired air. Although Butler and Stephenson (1988
) found that the heart rate of tufted ducks during diving was unaffected by the inspired gas composition in control and carotid-body-denervated ducks, dive heart rate was increased in carotid-body-denervated ducks irrespective of the gas mixture breathed beforehand. From these studies, it was generally concluded that carotid body chemoreceptors might play only a minor role in the control of cardiac responses to diving, at least under the circumstances investigated (short and shallow vertical dives).
In the present study, however, alteration of the oxygen content in the inspired air before diving produced strong and significant effects on the heart rate response during shallow (horizontal) and deep (vertical) diving. It might be argued that, because dive duration in the duck studies was short, a full chemoreceptor response could not develop. However, the differences in heart rate response of cormorants to alteration of inspired gas composition were established early during shallow diving (Fig. 6). In the case of hypoxic exposure before deep diving, the difference was established even before submersion (Fig. 7). Butler and Stephenson (1988) found that in an experimental set-up in which tufted ducks performed extended horizontal dives an almost identical situation to our cormorants performing shallow dives the bradycardia during diving was significantly slowed following carotid body denervation. Hence, they concluded that, under these circumstances, carotid body chemoreceptors might become more important.
Exposure to hypoxia effectively reduced pre- and post-dive heart rates of double-crested cormorants, although this effect was significant only for the deep diving situation, where the level of hypoxia was more severe. This is unlike the situation in tufted ducks, where hypoxic exposure significantly elevated pre- and post-dive heart rates in both control and carotid-body-denervated birds (Butler and Stephenson, 1988). It seems, however, that, although breathing gas with a lowered oxygen content causes a consistent increase in pulmonary ventilation, the cardiovascular effects are variable, depending on species and the degree of arterial hypoxaemia and hypocapnia (Daly, 1997
).
Hypercapnia had no significant effect on the diving heart rate of double-crested cormorants (Fig. 5), which is similar to the situation found in Pekin (Anas platyrhynchos) and tufted ducks. Jones et al. (1982) reported that CO2 contributed little (approximately 20 %) to the bradycardia accounted for by the carotid bodies in forcibly submerged Pekin ducks, while the strongest contribution came from O2 (approximately 65 %). Similarly, Butler and Stephenson (1988
) found that hypercapnia had no effect on the diving heart rate of voluntarily diving tufted ducks. While their ducks showed a significant reduction in pre- and post-dive heart rates after hypercapnic exposure, this was not the case in our cormorants. This difference might be due to the stronger degree of hypercapnic exposure in the tufted duck study.
Dive behaviour
The dive patterns observed during voluntary shallow diving in the present study are very similar to dive patterns reported for double-crested cormorants foraging in the wild. Ross (1974) observed double-crested cormorants diving in water 1.57.9 m deep. Dive and surface interval duration were 25.1 and 10.3 s, respectively, resulting in a dive/pause ratio (which is generally used as an index of dive efficiency) of 2.43. While the dive durations of our cormorants during shallow and deep diving are longer than those reported for double-crested cormorants foraging in shallow catfish ponds (King et al., 1995
), they are much shorter than the maximum dive duration (70 s) reported for this species (Munro, 1927
). A wide range of dive/pause ratios (between 1.95 and 4.36) was reported by Cooper (1986
) in his review of the diving patterns of 19 Phalacrocorax species. In the majority of Phalacrocorax species, however, dive duration during foraging typically exceeds the subsequent surface interval by a factor of 23 (Ross, 1974
; Cooper, 1986
; Ainley et al., 1990
), except for very low dive/pause ratios (0.30.4) reported for South Georgian shags diving to great depth (maximum 116 m) (Croxall et al., 1991
).
Dive durations in the present study did not differ during shallow and deep diving (Fig. 8). Why the birds increased the subsequent surface interval in the deep dive situation compared with the shallow dive situation is not easily explained. Since the birds were foraging on the same prey items (herring pieces), it is unlikely that increased surface times in the deep dive tank were associated with longer prey handling times. Considering the less dramatic cardiac changes associated with the deep diving situation, one could speculate about the functional significance of a dive bradycardia in facilitating efficient dive patterns. The rapid decline in heart rate observed during shallow diving presumably reflects the conservation of oxygen. If birds use less of their total oxygen store during the dive, they will be able to replenish these stores faster once ventilation resumes at the surface. A shorter post-dive surface interval would increase the proportion of the dive cycle spent under water and, hence, dive efficiency.
Alteration of inspired gas composition
Alteration of inspired gas composition (and hence blood gas tensions) had no effect on dive duration, which might be due to limitations of our experimental arrangement. Birds in both tanks did not have to chase prey under water but merely picked up a single herring piece and returned to the surface. Hence, the actual bottom time was relatively short, and dive duration was dictated by the transit time. Since only dives with an obvious foraging intention (i.e. birds swam to the feeding spot) were included in the analysis, it is not surprising to find that dive duration stayed constant irrespective of the composition of the breathing gas administered. With the dive duration being dictated by the experimental arrangement, birds were left only with the possibility of adjusting the duration of the subsequent surface interval. The adjustment of surface interval duration in accordance with the gas mixture administered (Fig. 8) clearly illustrates the importance of blood gas levels (O2 and CO2) in controlling the dive behaviour of double-crested cormorants.
This is similar to the situation reported for redhead and tufted ducks (Furilla and Jones, 1986; Butler and Stephenson, 1988
). The diving ducks in these studies, being stationary feeders that ingest food under water, could alter their food intake by adjusting dive duration (unlike the cormorants in our study). Accordingly, the dive duration of voluntarily diving redhead ducks increased as the level of O2 in the inspired air increased (Furilla and Jones, 1986
). In tufted ducks, dive duration decreased after hypoxic and after hypercapnic exposure, while hypercapnia increased the surface interval duration as well (Butler and Stephenson, 1988
). The dive efficiencies of double-crested cormorants in the present study follow the same general trend as those for tufted ducks: hypoxia and hypercapnia both decrease dive efficiency, while hyperoxia increases efficiency. The variance in dive/pause ratios in our study is probably explained by a change in recovery time in accordance with the O2 concentration in the inspired air. Refuelling O2 stores in a hypoxic environment will take longer than in a normoxic environment, necessitating longer surface intervals. Refuelling in a hyperoxic environment should be accelerated, decreasing surface interval duration. This might explain the short surface interval duration (resulting in the highest dive/pause ratio) after hyperoxic exposure in the shallow dive tank. Elevated heart rates during these dives (compared with the control) should lead to a greater O2 depletion, which would necessitate longer surface intervals to refuel O2 stores. The high O2 concentration in the inspired air, however, might allow for faster refuelling of the O2 stores, effectively reducing surface interval duration.
Butler and Stephenson (1988) suggested that surface interval duration is controlled primarily by CO2 concentration and that O2 concentration is the primary determinant of dive duration. Such a clear distinction is not possible in the present study because, given the experimental arrangement, the birds did not adjust their dive duration. Diving activity of ducks ceases at a critical O2 or CO2 concentration in the inspired air (Furilla and Jones, 1986
; Butler and Stephenson, 1988
). Similarly, when the O2 concentration in the inspired air fell below 8 %, our cormorants would not dive. The change in dive behaviour after hypoxic exposure in the deep dive situation was impressive. Surface interval duration increased by a factor of 4, resulting in a dive/pause ratio comparable with that of South Georgian shags performing much longer and deeper dives.
In conclusion, our study suggests that blood oxygen level is an important stimulus that allows double-crested cormorants to adjust their cardiac and behavioural system in accordance with the physiological restraints imposed during foraging. We propose that carotid body chemoreceptors, sensing arterial oxygen tensions, are the most likely mechanism facilitating the observed cardiac and behavioural responses. It is possible that these cardiac and behavioural adjustments to diving enable double-crested cormorants to maximise the time spent under water and, hence, potential foraging time.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Ainley, D. G., Strong, C. S., Penniman, T. M. and Boekelheide, R. J. (1990). The feeding ecology of Farallon seabirds. In Seabirds of the Farallon Islands (ed. D. G. Ainley and R. J. Boekelheide), pp. 51127. Stanford, CA: Stanford University Press.
Andrews, R. D. (1998). Instrumentation for the remote monitoring of physiological and behavioral variables. J. Appl. Physiol. 85, 19741981.
Ashmole, N. P. (1971). Sea bird ecology and the marine environment. In Avian Biology, vol. 1 (ed. D. S. Farner and J. R. King), pp. 223286. New York, London: Academic Press.
Bannasch, R., Wilson, R. P. and Culik, B. (1994). Hydrodynamic aspects of design and attachment of a back-mounted device in penguins. J. Exp. Biol. 194, 8396.
Bevan, R. M., Boyd, I. L., Butler, P. J., Reid, K., Woakes, A. J. and Croxall, J. P. (1997). Heart rates and abdominal temperatures of free-ranging South Georgian shags, Phalacrocorax georgianus. J. Exp. Biol. 200, 661675.
Butler, P. J. and Jones, D. R. (1997). Physiology of diving in birds and mammals. Physiol. Rev. 77, 837899.
Butler, P. J. and Stephenson, R. (1988). Chemoreceptor control of heart rate and behaviour during diving in the tufted duck (Aythya fuligula). J. Physiol., Lond. 397, 6380.[Abstract]
Butler, P. J. and Woakes, A. J. (1976). Changes in heart rate and respiratory frequency associated with spontaneous submersion of ducks. In Biotelemetry III (ed. T. B. Fryer, H. A. Miller and H. Sandler), pp. 215218. New York, San Francisco, London: Academic Press.
Butler, P. J. and Woakes, A. J. (1979). Changes in heart rate and respiratory frequency during natural behaviour of ducks, with particular reference to diving. J. Exp. Biol. 79, 283300.
Butler, P. J. and Woakes, A. J. (1982a). Control of heart rate by carotid body chemoreceptors during diving in tufted ducks. J. Appl. Physiol. 53, R1405R1410.
Butler, P. J. and Woakes, A. J. (1982b). Telemetry of physiological variables from diving and flying birds. Symp. Zool. Soc. Lond. 49, 107128.
Butler, P. J. and Woakes, A. J. (1984). Heart rate and aerobic metabolism in Humboldt penguins, Spheniscus humboldti, during voluntary dives. J. Exp. Biol. 108, 419428.[Abstract]
Calder, W. A. (1968). Respiratory and heart rates of birds at rest. Condor 70, 358365.
Cooper, J. (1986). Diving patterns of cormorants Phalacrocoracidae. Ibis 128, 562570.
Croxall, J. P., Naito, Y., Kato, A., Rothery, P. and Briggs, D. R. (1991). Diving patterns and performance in the Antarctic blue-eyed shag Phalacrocorax atriceps. J. Zool., Lond. 225, 177199.
Culik, B. (1992). Diving heart rates in Adélie penguins (Pygoscelis adeliae). Comp. Biochem. Physiol. 102A, 487490.
Daly, M. de B. (1997). Peripheral Arterial Chemoreceptors and RespiratoryCardiovascular Integration. Monographs of the Physiological Society no. 46. Oxford: Clarendon Press. 739pp.
De Leeuw, J. J., Butler, P. J., Woakes, A. J. and Zegwaard, F. (1998). Body cooling and its energetic implications for feeding and diving of tufted ducks. Physiol. Zool. 71, 720730.[Medline]
Elsner, R., Wartzok, D., Sonafrank, N. B. and Kelly, B. P. (1989). Behavioral and physiological reactions of arctic seals during under-ice pilotage. Can. J. Zool. 67, 25062513.
Enstipp, M. R., Andrews, R. D. and Jones, R. D. (1999). Cardiac responses to first ever submergence in double-crested cormorant chicks (Phalacrocorax auritus). Comp. Biochem. Physiol. 124A, 523530.
Furilla, R. A. and Jones, D. R. (1986). The contribution of nasal receptors to the cardiac response to diving in restrained and unrestrained redhead ducks (Aythya americana). J. Exp. Biol. 121, 227238.[Abstract]
Furilla, R. A. and Jones, D. R. (1987). The relationship between dive and pre-dive heart rates in restrained and free dives by diving ducks. J. Exp. Biol. 127, 333348.
Harrison, R. J. (1960). Experiments with diving seals. Nature 188, 10681070.[Medline]
Hertel, H. (1969). Hydrodynamics of swimming and wave-riding dolphins. In The Biology of Marine Mammals (ed. H. T. Andersen), pp. 3163. New York: Academic Press.
Johnsgard, P. A. (1993). Cormorants, Darters and Pelicans of the World. Washington, London: Smithsonian Institution Press. 445pp.
Jones, D. R. and Larigakis, S. (1988). The effect of breathing oxygen and air on diving bradycardia in cormorants (Phalacrocorax auritus). J. Exp. Biol. 136, 499502.[Medline]
Jones, D. R., Milsom, W. K. and Gabbott, G. R. J. (1982). Role of central and peripheral chemoreceptors in diving responses of ducks. Am. J. Physiol. 243, R537R545.[Medline]
Kanwisher, J. W., Gabrielsen, G. and Kanwisher, N. (1981). Free and forced diving in birds. Science 211, 717719.[Medline]
King, D. T., Glahn, J. F. and Andrews, K. J. (1995). Daily activity budgets and movements of winter roosting double-crested cormorants determined by biotelemetry in the Delta region of Mississippi. In The Double-Crested Cormorant: Biology, Conservation and Management (ed. D. N. Nettleship and D. C. Duffy). Col. Waterbirds 18 (special publication 1), 152157.
Kooyman, G. L. (1989). Diverse Divers: Physiology and Behavior. Berlin, Heidelberg: Springer Verlag. 200pp.
Kooyman, G. L., Schroeder, J. P., Greene, D. G. and Smith, V. A. (1973). Gas exchange in penguins during simulated dives to 30 and 68 m. Am. J. Physiol. 225, 14671471.
Lanphier, E. H. and Rahn, H. (1963). Alveolar gas exchange during breath-hold diving. J. Appl. Physiol. 18, 471477.
Lovvorn, J. R. and Jones, D. R. (1994). Biomechanical conflicts between adaptations for diving and aerial flight in estuarine birds. Estuaries 17, 6275.
Mangalam, H. J. and Jones, D. R. (1984). The effects of breathing different levels of O2 and CO2 on the diving responses of ducks (Anas platyrhynchos) and cormorants (Phalacrocorax auritus). J. Comp. Physiol. B 154, 243247.
Munro, J. A. (1927). Observations on the double-crested cormorant (Phalacrocorax auritus) on Lake Manitoba. Can. Field-Nat. 41, 102108.
Olszowka, A. J. and Rahn, H. (1987). Breath-hold diving. In Hypoxia and Cold (ed. J. R. Sutton, C. S. Houston and G. Coates), pp. 417428. New York: Praeger.
Qvist, J., Hill, R. D., Schneider, R. C., Falke, K. J., Liggins, G. C., Guppy, M., Elliott, R. L., Hochachka, P. W. and Zapol, W. M. (1986). Hemoglobin concentrations and blood gas tensions of free-diving Weddell seals. J. Appl. Physiol. 61, 15601569.
Qvist, J., Hurford, W. E., Park, Y. S., Radermacher, P., Falke, K. J., Ahn, D. W., Guyton, G. P., Stanek, K. S., Hong, S. K., Weber, R. E. and Zapol, W. M. (1993). Arterial blood gas tensions during breath-hold diving in the Korean ama. J. Appl. Physiol. 75, 285293.[Abstract]
Robertson, I. (1974). The food of nesting double-crested and pelagic cormorants at Mandarte Island, British Columbia, with notes on feeding ecology. Condor 76, 346348.
Ross, R. K. (1974). A comparison of the feeding and nesting requirements of the great cormorant (Phalacrocorax carbo L.) and double-crested cormorant (P. auritusLesson) in Nova Scotia. Proc. N.S. Inst. Sci. 27, 114132.
Stephenson, R. (1994). Diving energetics in lesser scaup (Athyta affinis, Eyton). J. Exp. Biol. 190, 155178.
Stephenson, R., Butler, P. J. and Woakes, A. J. (1986). Diving behaviour and heart rate in tufted ducks (Aythya fuligula). J. Exp. Biol. 126, 341359.[Abstract]
Wanless, S., Harris, M. P. and Morris, J. A. (1992). Diving behaviour and diet of the blue-eyed shag at South Georgia. Polar Biol. 12, 713719.