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Blood volume distribution in and bioenergetics of swimming and diving ducks Heieis, Mark Rudolf Alois 1987

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B L O O D V O L U M E DISTRIBUTION IN A N D B I O E N E R G E T I C S O F SWIMMING A N D DIVING D U C K S by Mark Rudolf Alois Heieis B.Sc, University of British Columbia, 1982 A THESIS SUBMITTED LN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in THE FACULTY OF GRADUATE STUDIES (DEPARTMENT OF ZOOLOGY) We accept this thesis as conforming to the required standard The University of British Columbia October 1987 c Mark Rudolf Alois Heieis, 1987 In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the head of my department or by his or her representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. The University of British Columbia 1956 Main Mall Vancouver, Canada . V6T 1Y3 \ s Department of DE-6(3/81) Abstract Blood flow distribution during forced and voluntary diving in ducks, and the energetic cost of diving was investigated. It has been suggested that in order for the leg muscles to generate enough power for ducks to dive, blood flow to those tissues must be maintained. A technique to determine blood flow distribution which could be used during voluntary diving was first developed and tested during forced laboratory dives of ducks. This technique was then used to determine the blood flow distribution during voluntary diving. Regional blood flow distribution was visualized by utilizing a radioactive tracer technique (macro aggregated albumin labelled with 99mtechnetium). The tracer when injected into an animal is trapped and held by capillaries. During forced dives in dabbling (A TICS platyrhynchos) and diving (Aythya affinis) ducks the blood flow distribution was found to be restricted to the thoracic and head areas. Whereas during a voluntary dive in A. affinis blood flow distribution was shown to be preferentially directed towards three tissue areas, the heart, brain, and active leg muscles. The work required to dive was determined from the measurement of subsurface drag forces and buoyancy in A. affinis. Subsurface drag increased as a nonlinear function of swimming velocity. At a velocity of 1 nrs"1, the drag force was approximately 1.067 N. The average measured buoyant force of 11 ducks was 0.953 N. The calculated mechanical work done by ducks during a 14.4 s unrestrained dive was 9.34 J. The power output during voluntary was estimated to be 0.751 W (0.0374 ml 02"S"1). During diving buoyancy is clearly the dominant force (8.8 J) against which ducks have to work while drag (0.54 J) adds little (~6%) to the energetic cost of diving. ii Table of Contents L i s t of Figures v L i s t of Tables v i Acknowledgements v i i GENERAL INTRODUCTION 1 CHAPTER 1. Blood Flow and Volume D i s t r i b u t i o n During Forced Submergence i n Pekin Ducks (Anas Platyrhynchos) Introduction .. 4 Methods (a) General Methods, Monitoring of Cardiovascular Var iables , & Analysis of data 6 (b) Blood Flow D i s t r i b u t i o n Methods and Procedure 7 i . S t a t i c Studies 7 i i . Dynamic Studies 8 i i i . Gamma Camera Equipment &. Scanning Procedure • 9 (c) Blood Volume Determinations 10 Results 1. Relat ive Blood Flow D i s t r i b u t i o n During Forced Submergence 12 2. Time A c t i v i t y Curves of Bolus Injected 99mTc Labelled RBCs During Rest and Forced Submergence 12 3- Vascular Volume Changes During Forced Sumergence 14 4. Blood Volume D i s t r i b u t i o n During Rest and Forced Submergence 14 Discussion 26 CHAPTER 2. Blood Flow D i s t r i b u t i o n During Voluntary D i v i n g i n a D i v i n g Duck (Aythya a f f i n i s ) I n t r o d u c t i o n 29 Methods 30 R e s u l t s 32 D i s c u s s i o n 35 CHAPTER 3. The B i o e n e r g e t i c s of Surface and Subsurface Swimming i n D i v i n g Ducks (Aythya a f f i n i s ) I n t r o d u c t i o n 36 Methods (a) Buoyancy Measurements 38 (b) Surface & Subsurface Drag Measurements 39 (c) S t a t i s t i c s 40 R e s u l t s 1. Buoyancy and Body Volume 4 l 2. Surface and Subsurface Drag Meaurements 42 D i s c u s s i o n 48 GENERAL DISCUSSION 52 APPENDIX 1. I n f u s i o n Pump Pack 57 REFERENCES CITED 58 i v Lis t of Figures Figure 1.1 Blood Flow Distribution in Dabblers 16 Figure 1.2 Time Act iv i ty Curves During Rest 17 Figure 1.3 Time Act iv i ty Curves During Forced Submersion 19 Figure 1.4 Time Act iv i ty Curves of Veno-Venous Shunt . . 21 Figure 1.5 Vascular Volume Changes During Forced Submergence 23 Figure 2.1 Blood Flow Distribution During Voluntary Diving 33 Figure 3 • 1 Buoyant Force of a Duck 43 Figure 3-2 Relationship between Body Mass & Volume . . . . 45 Figure 3-3 Surface & Subsurface Drag Force Curves 46 Figure 3-4 Comparison of Surface & Corrected Subsurface Drag 51 v Lis t of Tables Table 1.1 Circulating Blood Volume 25 Table 3-1 Buoyancy and Volume Values 44 Table GD.I Aerobic Efficiency of Surface Swimming 56 v i Acknowledgements I thank Dr. David R. Jones for providing me with the opportunity and facilities to carry out my reseach program. I also thank my colleagues in the lab of Dr. Jones, especially Drs G. Gabbott and R. Stephenson. This study was supported by grants from the British Columbia Heart Foundation and N.S.E.R.C.C. awarded to Dr. Jones. vii General Introduction It is well established that in response to forced submersion animals produce a series of oxygen conserving measures to prolong their survival (Scholander, 1940; Irving et al, 1942; Andersen, 1966). These responses include bradycardia and vascular constriction which result in a general decrease in peripheral blood flow. This provides a means by which blood oxygen is conserved for use by obligate aerobic tissues, such as the heart and brain. In 1960, Eliassen questioned whether or not these responses had any siginificance during free range voluntary dives by animals. He reasoned that because most voluntary dives in the wild lasted only a few minutes, and because he did not detect a reduction of metabolic rate in birds within the first few minutes of a forced dive in the laboratory, vasoconstriction most likely did not occur. Andersen (1966) contested Eliassen's proposal, claiming that a reduction of metabolic rate was merely a consequence of the massive peripheral vasoconstriction that develops during the initial period of a long dive. Therefore, metabolism could not be used to indicate what vascular changes are occurring during diving. Scholander and Irving had already expressed doubts that there would be much lactic acid produced during the short dives normally made by seals, and wondered how muscles isolated from the circulation could maintain their "capacity for activity" (Scholander et al., 1942). It is now widely accepted that there are some major differences between the type of responses elicited during prolonged laboratory forced dives and of those during free range voluntary diving (Millard et al., 1973; Butler, 1982; Woakes and Butler, 1983). Millard et al. (1973) suggested that the cardiovascular adjustments seen during voluntary diving were a result of two diametrically opposed physiological responses acting at the same time, those of aerobic exercise (tachycardia, hyperpneoa, increased 1 blood flow to active tissues) and forced diving (bradycardia, apneoa, reduced peripheral blood flow). They showed that blood flow to muscle and cardiac output had only minor decreases during voluntary diving as compared with the massive changes seen in penguins during forced dives. It has been postulated that the vascular responses during diving are biased towards those of exercise (Millard et al, 1973; Butler, 1982). As a result, comparative physiologists are now striving to characterize the cardiovascular responses diving animals elicit and their energetic requirements during free range voluntary dives. Telemetry of heart rate has been extensively used and has enabled numerous observations of the nature of cardiac responses to voluntary diving (Millard et al, 1973; Butler and Woakes, 1979; Woakes and Butler, 1983; Furilla and Jones, 1985). Unfortunately, heart rate provides only an indirect indication of the overall cardiovascular state, such as cardiac performance, blood flow or distribution. Heart rate has, however, been shown to be linearly related to oxygen demand during exercise in normally ventilating birds (Woakes and Butler, 1983), and V Q 2 is also related to the level of exercise in normally ventilating birds and mammals (Taylor et al, 1982; Woakes and Butler, 1983 & 1986). If the level of heart rate is indicative of metabolism, then metabolism in diving ducks during volunary diving may be elevated as well, since heart rate during voluntary diving has been shown to be much higher than in forcibly submerged ducks (Butler and Woakes, 1979; Furilla and Jones, 1985; Woakes and Butler, 1986; Stephenson et al, 1986). Metabolism was, in fact, shown to be 3.5X higher during unrestrained diving in tufted ducks than at rest, but it was also shown that heart rate was not related to oxygen consumption during voluntary diving in the same way as it is during surface exercise (Woakes and Butler, 1983). Therefore, heart rate cannot be used as an accurate indicator of metabolism or the amount of work being 2 done during voluntary diving (Woakes and Butler, 1983). However, the high estimate of oxygen consumption during unrestrained dives in ducks still suggests that the power output required to dive is high. As yet, there has been no measure of the work required to dive by ducks. . It has also been suggested that in order for the locomotory muscles to maintain a high level of power output during voluntary diving, blood flow to the active leg muscles is most likely maintained (Millard et al, 1973; Butler 1982; Woakes and Butler, 1983). This is contrary to what is found in forcibly submerged ducks where blood flow to all skeletal muscle tissues is greatly reduced (Jones et al, 1979). To date there have been no direct measurements of either blood distribution or blood flow changes during voluntary diving in ducks. The primary goals of this study were to ascertain the location of the blood volume and blood distribution during voluntas dives in ducks and to determine the energetic cost of diving for ducks. Techniques developed to monitor blood flow distribution in forcibly submerged ducks have been adapted for investigations of blood flow distribution in unrestrained diving ducks. Dynamic changes of blood flow and blood volume distribution were also investigated in forcibly submergered ducks. Finally, the energetic cost of voluntary diving was estimated from the measurement of subsurface drag and buoyant forces which oppose ducks when diving. 3 Chapter 1 BLOOD FLOW AND VOLUME DISTRIBUTION DURING FORCED SUBMERGENCE IN PEKIN DUCKS (Anas platyrhynchos) INTRODUCTION During forced submergence, diving birds and mammals display bradycardia and a massive peripheral vasoconstriction. The latter eliminates blood flow to hypoxia insensitive tissues so that lung and blood oxygen stores are saved for the heart and brain, both of which are crucially dependent on a continued oxygen supply. It is possible that due to this massive vasoconstriction a significant proportion of the total blood volume could be isolated from that which circulates to the heart and brain in the dive. In fact, Murphy et al. (1980) suggested that, in seals, less than 15% of the total blood volume was effectively circulated, while the remaining 85% was in the 'peripheral circulation' and was only slowly exchanged with the circulating blood. In Pekin ducks, approximately 50% of non-myoglobin-bound oxygen is carried in the blood, while the remaining amount is stored in the lung and air sac system (Hudson & Jones, 1986). During forced submergence, Pekin ducks use approximately 75% of the oxygen contained in the respiratory system (Hudson & Jones, 1986) and almost all of the blood oxygen so the contribution of the blood oxygen store to the survival of the animal is proportionally greater than is suggested by pre-dive oxygen storage distribution (Jones & Furilla, 1987). Consequently, during forced submergence, it would seem disadvantageous for the animal to isolate such a large part of its major oxygen store from its vital (oxygen dependent) tissues. 4 In non-marine mammals, approximately 20% of the total blood volume is located in the arteries, small arteries, arterioles, capillaries, and post-capillary venules, while the remaining 80% is divided almost equally between the venules, small veins, and large veins (Wiedeman, 1963). Therefore, if the pre- and post-capillary areas of all tissues except the heart and brain were instantaneously isolated from the circulation, one might hypothesize that most of the total blood volume would be available to yield its crucial oxygen supply in a dive, as long as the blood contained within the central venous system was being circulated. The intent of this study was to test this hypothesis, and to determine how blood flow and blood volume distribution contribute to maximal utilization of the blood oxygen store. 5 METHODS (a) General Methods, Monitoring of Cardiovascular Variables, & Analysis of Data. Experiments were done at room temperature (20-24°C) on unanaesthetized white Pekin ducks (Anas platyrhynchos) ranging in body mass from 2 to 3 kg. All surgical procedures were of a minor nature and were carried out under local anesthesia (2% lidocaine hydrochloride; Astra Pharmaceuticals, Toronto, Ont). The left brachial artery was cannulated with PE 90 tubing and one or both brachial veins with PE 190. The cannulae were filled with saline containing 50 USP units'ml"1 Heparin (Glaxo Canada, Toronto, Ont). The arterial cannula was advanced until the tip was either in the left ventricle or at the base of the aortic arch, proximal to the aortic valve. The venous cannulae were advanced some 10 to 15 cm until their tips lay in the great veins. Cannulae were Filled with X-ray opaque material and the location of their tips in the cardiovascular system was confirmed by radiography. The ducks were restrained on an operating table for blood volume studies, and on a plexiglass template shaped in the form of a duck for gamma scanning studies. In the former, the animal's head was restrained by a plexiglass assembly which could be lowered into a container of water to start a dive. Forced dives in the gamma scanning studies were done by immersing the duck's head, manually, into a beaker of water. Arterial blood pressure was monitored from the brachial artery cannula using a Biotec BT-70 (Narco Biosystems, Houston, TX, USA) pressure transducer. Blood pressure traces were recorded, using rectilinear coordinates, on a 2 channel chart recorder. Heart rate was obtained from the blood pressure traces. Values are given as means ± standard error of the mean (SEM). Paired t-tests were used to determine significant differences (P<0.01) between paired sets of data. 6 (b) Blood Flow Distribution Methods & Procedure. Blood flow distribution was visualized using static and dynamic distribution techniques. In static studies, blood flow distribution was determined by organ trapping of gamma labelled Macro Aggregated Albumin (MAA) (Frosst Pharmacueticals, Kirkland, Quebec). The MAA technique is similar to the glass microsphere technique in that the MAA is trapped and held in the capillary circulation, and the gamma scan reveals the blood flow distribution. In the dynamic studies, the movement of gamma labelled red cells was observed over time. In both studies, the gamma emitting radionuclide used was """technetium (99mTc) which was generated from 99molybdenum (99Mo) (Minitec, Frosst Pharmacueticals, Kirkland, Quebec). The physical half-life of the radionuclide is 6.02 hours. (i) Static Studies. Nine ducks were injected with 9 9 mTc labelled MAA. First, a low dose of approximately 4 MBq of MAA in a volume of 1 to 2 ml was injected slowly via the arterial cannula into ducks, 2 minutes after the start of a forced dive. Following the dive scan, a second and much higher 40 MBq dose of MAA, 1 to 2 ml, was injected to obtain blood flow distribution during rest either within the same scan session or 24 hours later. The injected MAA is trapped at the first capillary bed and remains trapped for approximately 2 hours before being broken down. Consequently, the animal can be injected and scanned again 24 hours later, or alternatively, repeated injections of MAA can be made under different experimental conditions with little time between scans, provided the subsequent activity dose is approximately 10X higher than the previous dose. The average particle size of the MAA was 40 Jim. 7 (ii) Dynamic Studies. Dynamic studies were performed on 14 ducks. Red blood cells, withdrawn from the duck about to be scanned, were labelled in vitro with 9 9 mTc as follows; 0.3 ml of gluceptate (Frosst Pharmaceuticals, Kirkland, Quebec) was injected into the duck via the arterial cannula and 15 minutes later, 6 ml of blood was withdrawn. Haematocrit was determined by microcapillary technique. One millilitre of anticoagulant, acid-citrate-dextrose (ACD) solution (dextrose 132 mg, sodium citrate 250 mg, citric acid 80 mg, water 10 ml), and 400 MBq of 9 9 n Tc were added to the blood sample which was then incubated for 10 minutes at room temperature. After centrifugation and separation, both plasma and RBC fractions were counted by a dose-calibrator (Picker, Northford, CT, USA) to determine the amount of 9 9 mTc labeling. The amount of free 9 9 mTc in the plasma was usually less than 5%. The RBC fraction was then resuspended to the haematocrit of the blood sample with physiological saline. Approximately 2 ml ( — 80 MBq) of 9 9 mTc tagged RBCs were used for bolus injection. To obtain time-activity curves of injected tracers, 2 ducks were injected 2 minutes after the start of a dive with labelled RBCs. The dive duration for these animals was 7 minutes. Three ducks were injected with a 2 ml bolus of labelled RBCs during rest. These animals were scanned from the start of the injection for 10 minutes. In one duck, a veno-venous shunt was made in an effort to determine the rate at which injected radioactivity mixed in the circulation. Both right and left brachial veins were cannulated. Blood was pumped from left to right through the extra-corporeal circuit by a Wiz pump/diluter/dispenser (Isco, Lincoln, NE, USA) at a rate of 2 ml'mur1. Labelled RBCs were injected over a 60 s period through the pump. To observe changes in vascular capacitance, """technetium labelled red blood cells were injected into 7 ducks 10 to 20 minutes before a dive. This was done to ensure 8 that the labelled RBCs had completely mixed within the animal's cardiovascular system. The ducks were scanned while held in the dive position before, during, and after 4 minute dives. (iii) Gamma Camera Equipment & Scanning Procedure. The gamma scanning instruments used in both static and dynamic scans were a Picker Dyna Camera 4/15 with attached Micro Z processor, Image Programmer, and Dyna Camera 4 controller (Picker, Northford, CT, USA). Real time image data acquisition, processing, and analysis were done with a micro processor system, Adac DPS-2800 (Adac Laboratories, Sunnyvale, CA, USA), interfaced to the gamma camera using Adac's Nuclear Medicine System, V2A software. The resolution of the combined detector and computer systems was 3 mm. Image size was 128 x 128 pixels x 8 bits in both static and dynamic scan studies. During scanning experiments, digital images were acquired at a rate of 1 image'second"1 for 10 min. At the end of each scan, the computer was used to select regions of interest from a displayed digital image. The activity in the various regions of interest on each image at a given time was counted, processed and plotted. Unfortunately, since the gamma scanning equipment yields a two dimensional image from a 3 dimensional object, it can not provide quantitative flow data. Consequently, in an attempt to obtain quantitative blood flow data, two ducks were scanned using a 3 dimensional (rotational) gamma camera, but because of the poorer effective resolution of rotational gamma camera further studies were not pursued using this instrument. Serial photographic images of the ducks were also taken on X-ray plates, as the labelled cells were injected into a duck, at a rate of 2 seconds^ image"1 for 32 s during dynamic scans, whereas for static scans, single digital and photographic images were acquired per scan. 9 (c) Blood Volume Determinations. Total red blood cell (RBC) volume was determined in 5 ducks by labelling the cells with 51chromium (51Cr). Approximately 6 ml of blood was withdrawn from the brachial artery. Arterial haematocrit was determined by the microcapillary technique. In eight ducks, arterial haematocrit was monitored before and during dives of up to 4 minutes in duration. In 2 ducks, arterial haematocrit was measured before and during dives in which RBC volume was also measured. One millilitre of ACD and approximately 1.5 MBq of sodium51dichromate (51Cr) were added to the blood sample. The blood-ACD-51Cr solution was then gently mixed and incubated for 25 minutes at room temperature. During this period the chromium, which is in a hexavalent state, freely passes into the red cells where it binds to haemoglobin and is thereby reduced to a trivalent state which cannot pass through the cell membrane. After incubation, approximately 25 mg of L-ascorbic acid was added to the solution to stop the tagging process. This procedure reduces any free chromium present in the incubating solution, or within the red cells, thereby preventing any further movement of 51Cr into or out of the RBC. The solution was incubated and gently agitated for a further 10 to 15 minutes. The labelled cells were then washed 2 or 3 times with saline. Tagged red cells were resuspended in saline and haematocrit was determined for the resuspended cells. Two millilitres of the suspension was then withdrawn into a syringe for injection into the animal. Standards were prepared from the resuspended solution and, after centrifugation, from the suspension saline. Five 100 jil aliquots of both the resuspended RBCs (injection standard) and suspension saline (saline standard) were counted in a Picker Pace II gamma counter (Picker, Northford, CT, USA). The average count for the 5 aliquots of the resuspended RBCs and suspension saline was obtained. 10 Labelled RBCs were injected into the ducks through the venous cannula 1 to 2 minutes after the start of a dive. Arterial blood samples (2 ml) were taken 2 to 5 minutes after injection and then 20 minutes post-dive. Five aliquots of whole blood (whole blood sample) and 5 aliquots of plasma (plasma sample), each of 100 yl, for both dive and post dive samples were counted. The average count of both sets of 5 aliquots was taken and used, along with the injection and saline standards, in the following formula to calculate total red cell volume. volume injected X [injection std - (saline std X Plet(injection std))] RBC volume = , , , , , , , „ „ , . , , . , „ X Arterial Hct whole blood sample - (plasma sample X Plct(artenaD) where: std = standard Hct = Red Cell Volume/Total Blood Volume Plct = decimal plasmacrit = 1 - Hct 11 RESULTS 1. Relative Blood Flow Distribution During Rest & Forced Submergence. Relative blood flow distribution was obtained under resting and forced dive conditions in 9 ducks. Composite images of a single duck are presented in Figure 1.1. The arbitrary colour scale on the left indicates relative blood flow with regions of high blood flow being red-white and regions with low blood flow being blue (figure 1.1). During rest (heart rate = 276 beats^ minute-1) blood flow was widely distributed with the lower abdominal and visceral areas having the highest relative flows (figure 1.1-REST). During forced diving, even when dive heart rate was 60 beats'minute"1, blood flow was restricted largely to the thoracic and head areas (figure 1.1-DIVE). 2. Time Activity Curves of Bolus Injected 9 9 mTc Labelled RBCs During Rest and Forced Submergence. Ducks were scanned as ""technetium labelled red blood cells were injected arterially during rest and diving (figures 1.2 & 1.3). In resting animals labelled blood cells were distributed throughout the animal within 30 seconds as indicated by the activity reaching a stable level in the head, leg, thoracic, and visceral areas within this time (figure 1.2a,b&c). The arterial distribution of the bolus was variable and was dependent on the rate and smoothness of injection and how fast the cannula was flushed. Activity would be expected to appear in the central cardiovascular area first since the labelled cells enter via a cannula in this area, but even with a higher resolution of the time base this was not usually obvious (figure 1.2b&c). However, in the one animal in which activity in the head region was monitored, appearance of activity in the head region was delayed for 10-15 s, although this might not be a typical result (figure 1.2b). 12 A bolus of 9 9 mTc labelled RBCs injected 2 minutes after the start of a dive gave simultaneous increases in activity in all of the observed regions (figure 1.3). Peak activity occurred first in the head area, with peak activity in the thoracic area being reached as the bolus returned from peripheral areas. In the head and chest regions, the activity equilibrated within 2 minutes (figure 1.3a&b). However, activity continued to increase in the visceral tissue areas throughout the dive, although activity in the legs appeared to reach a stable level some 3-4 min after injection (figure 1.3a&b, legs & viscera). Immediately after surfacing, activity in the thoracic area fell, and a second and final equilibrium plateau was reached (figure 1.3), while activity increased in the leg and visceral regions. Activity in the head region appeared to fall post-dive, but this cannot be confirmed with the present data because the head had to be moved to terminate the dive which caused an abrupt drop in activity. Repositioning of the head after emergence was probably not exact, making comparisons of post-dive and dive levels inaccurate. A similar pattern of labelled RBC distribution was seen when RBCs were injected via the veno-venous shunt, although the appearance of activity in peripheral regions was somewhat delayed (figure 1.4) compared with arterial injection (figure 1.3). This is probably due to the slow injection of the labelled RBCs (1 min). In the thoracic area, peak activity was reached approximately 30 s after the last of the 9 9 mTc RBCs had been injected. Activity subsequently fell and reached a steady level 2 minutes after the peak. Activity decreased in the veno-venous shunt (figure 1.4c), while it continued to increase in the visceral and leg areas (figure 1.4b) in the dive. Upon termination of the forced dive, activity in the thoracic region fell, while the activity in the visceral & leg regions increased. These changes were similar to those observed in figure 1.3. There was no discernable change in activity in the extra-corporeal shunt post-dive (figure 1.4c) 13 because background activity levels were higher than any radioactivity contained within the shunt. 3. Vascular Volume Changes During Forced Submergence. In seven ducks, 9 9 mTc labelled RBCs were injected 10-20 minutes before submergence. During a 4 minute dive, the activity in the abdominal and leg areas decreased, indicating a reduction in the number of labelled RBCs in these regions (figure 1.5) while the activity in the thoracic area increased indicating an increase in labelled RBCs in this area (figure 1.5). At the start of the forced dive, activity levels usually dropped faster in the visceral than in the leg area (Figure 1.5). At the termination of the dive, counts in all three areas returned to resting levels although activity in the leg region appeared to return to resting much faster than in the other two regions (figure 1.5). More than one dive was performed with each duck and, except for a predicted reduction in overall levels of activity due to radioactive decay, qualitatively similar results were obtained on subsequent dives (figure 1.5c&d). 4. Blood Volume Distribution During Rest & Forced Submergence. The average red cell volume in 5 resting animals determined 20 minutes after diving was 28.01 ± 0.44 ml RBCs'kg(BM)1 (table 1.1). During submergence, however, the average circulating red cell volume was measured at 21.05 ± 1.24 ml RBCs^kgfBM)-1. The difference between post-dive and dive values is statistically significant. Circulating red cell volume during forced submergence varied from a low of almost 65% to a high of 90% with an average of 75.2 ± 4.6 % of the red cell volume circulating after recovery from the dive. Arterial haematocrit was also measured in 10 ducks before and during forced dives. There were no significant changes in arterial 14 haematocrit in the dive (0.404 ± 0.007) compared with pre-dive values (0.403 ± 0.006). 15 Figure 1.1. Blood flow distribution in a resting (REST) and forcibly submerged duck (DIVE) after 2 min. The image is a composite of 2 scans, one for the body and one for the head. Each region was scanned for exactly the same length of time. The time between scans was just that required to reposition the duck. The colour scale indicates the relative level of blood flow (red = high flow, blue = low flow). During rest, blood flow is widely distributed, whereas during diving, it is largely restricted to the heart and head. 16 16A Figure 1.2. Time activity curves of a bolus injection of 9 9 mTc labelled red blood cells into 3 ducks during rest (a,b,c). In (a) the time base is compressed while in (b) and (c) it is expanded (T = thorax, V = viscera, L=legs, H = head). 17 18 Figure 1.3 Time activity curves of a bolus injection of 9 9 mTc labelled red blood cells into 2 ducks (a&b) 2 minutes after the start of a forced dive. (T = thorax, V = viscera, L=legs, H = head, A=end-dive) 19 counts/min Time (s) Figure 1.4 Time activity curves of labelled red blood cells infused though a veno-venous shunt, (a) activity in the thorax (T), (b) activity in the viscera (V) and legs (L), (c) extra-corporeal shunt (E), and (A) = end-dive. 21 counts/min 22 Figure 1.5 Vascular volume changes during 4 minute forced dives determined from the distribution of labelled RBCs. Labelled red blood cells were injected some 20 min or more before the start of the scan. Scans (a), (b), & (c) are different ducks, while (b) & (d) are scans from the same duck apart. (T = thorax, V = viscera, L=legs, T =dive, A=end-dive). 23 24 Table 1.1 Total Red Blood Ce l l volume determined during rest (post -d ive) and during forced d ives . Body m1x1ng RBC volume %ci rcu1 at 1ng A r t e r i a l Hct Mass 11me (ml RBC/kg(BM)) during dive (post-dive) (kg) (min) pos t -d ive dive 2.7 2 27 . 17 24 . 29 89.57 0.460 2.6 2 28.61 23.22 81.15 0.378 2.4 2 27.00 18.90 70.00 0.432 2.7 4 29.33 21.11 71 .99 0.380 3.7 5 27 .95 17.75 63.49 0.432 mean values 2 8 . 0 1 ± 0 . 4 4 2 1 . 0 5 ± 1 . 2 4 75.24+4.5G 0.416+0.011 25 DISCUSSION These tracer studies have confirmed the pattern of blood flow distribution during rest and forced submergence in ducks determined by other methods (Jones et al., 1979); that is, 99mTc labelled macroagreggated albumin was trapped in capillaries giving a picture of blood flow distribution during dives that is almost entirely restricted to the heart and brain. This contrasts with results from the dynamic blood flow studies which showed that peripheral circulation of the blood also occurred during forced dives. In fact, the present study also showed that most of the total red cell volume was being circulated during forced submergence. Therefore, it would appear that forcibly submerged ducks make cardiovascular adjustments that position most of their oxygen stores in readily accessible locations for use by the brain and heart. Dynamic gamma scans of radioisotope-labelled red blood cells, injected either arterially or venously, two minutes into a forced dive showed that blood flow continued to the leg and visceral areas since radioactivity increased in these regions. If flow had ceased to these areas during the dive, the radioactivity would not have increased. Microsphere studies by Jones et al. (1979), indicated that blood flow to muscle was arrested during forced submergence in ducks. This was the same result that Djojosugito et al. (1969) found, but they also showed that blood flow to the webs was maintained. As a consequence of this maintained web flow, the distal venous blood store will be circulated while the skeletal muscle beds are bypassed. During the dive labelled RBCs whihc had been injected and mixed before the start of the dive decreased in the visceral and leg areas but increased in the thoracic area (figure 1.5). Radioactivity can increase or decrease (other than by radioactive decay) by a change in either flow rate or the number of red cells in that area. It is unlikely that there was an increase in overall blood flow rate in the central 26 cardiovascular area because cardiac output during forced submergence is greatly decreased while myocardial flow is largely unchanged (Jones and Holeton, 1972; Jones et al., 1979). Therefore, the only way radioactivity could rise is by an increase in the number of red blood cells in this region. In other words, the blood volume must be shifted from the peripheral to the central venous area during diving. Djojosugito et al. (1969) reported that blood was actively expulsed from skeletal muscle by venoconstriction, while Langille (1983) measured a marked increase in venous tone during forced submersion. The effect of these actions would be to reduce the vascular space in the peripheral veins and to shift the blood to the central venous compartment allowing most of the blood pool to be available to the heart and brain in dives. The dynamic tracing of radioactively labelled red blood cells injected during a dive showed that once initial mixing had taken place, little further mixing occurred with any isolated portion of the blood volume because activity levels in the central and even peripheral cardiovascular areas reached a plateau. This is opposite to what was suggested by Murphy et al. (1980) for seals. In ducks, there is a large central blood pool containing about 75% of the total blood volume (TBV) which mixes only slightly with the 25% of TBV located in the hypoperfused tissues during a dive. In recovery, activity increased in the peripheral regions while it fell in the central cardiovascular area. These changes represent not only flow and volume redistribution in the post-dive period, but also a dilution factor due to the increase in total circulating blood volume. Furthermore, arterial haematocrit did not change in dives, unlike that reported for some seals (Qvist et al., 1986). This is not unexpected because in ducks the spleen is extremely small (Nickel et al., 1977) and therefore cannot function as a reserve of oxygenated red blood cells during diving. 27 Time-activity curves of labelled RBC tracers injected either arterially or venously revealed that the time to reach an equilibrium during diving was at least 4 to 10 times longer for central and peripheral regions respectively than when RBCs were injected during rest. In ducks, this is a reflection of the reduction in cardiac output during diving rather than mixing with peripherally located pools of blood. The time taken to attain equilibrium during diving has important implications with regard to the use of tracers and metabolites in diving studies. Most tracer studies require that the tracer be equilibrated throughout all of the animal's cardiovascular compartments before any statement can be made as to its distribution, metabolism, or disappearance. Consequent^ , results of such studies must be regarded with suspicion in the absence of an accurate measure of flow pattern and mixing time during diving (Castellini et al., 1985; Guppy et al, 1986). 28 Chapter 2 BLOOD FLOW DISTRIBUTION DURING VOLUNTARY DIVING IN A DIVING DUCK (Aythya affinis) ft INTRODUCTION It has been shown that the leg muscles of Pekin ducks cannot sustain a high level of activity without a blood supply during forced submersion (Jones et al., 1987). Unlike the situation for forced diving, power input (V02) is elevated during voluntary diving in the tufted duck (Woakes and Butler, 1983). In fact, it has been suggested that cardiovascular changes during voluntary diving are a compromise between those which occur during forced dives and those which occur during aerobic exercise in normally ventilating animals (Millard et al., 1973; Butler, 1982; Woakes & Butler, 1983). It has therefore, been suggested that during voluntary dives, active muscles are supplied with blood in order to meet the high energy requirement of submerged swimming. To date, a direct measurement of blood flow during voluntary diving in ducks has never been made. The main reason for this is the technical difficulty of devising methods which do not physically intervene with the duck to the extent of interfering with their natural diving behaviour. The intent of this study, therefore, was to develop a method to measure the blood flow distribution in free ranging ducks, and to investigate blood flow changes during voluntary diving compared with rest and forced dives. 29 METHODS Experiments were done on 2 Lesser Scaup (Aythya affmis) each weighing approximately 600 g. Ducks were trained to dive in a mesh-covered tank (3 x 5 x 0.5 m at the shallow end sloping to a depth of 1.5 m). After each duck was familiar with diving under the mesh, an 80 g 'dummy-pack' was securely fastened to its back with two body straps. The 'dummy-pack' had the same dimensions and mass as the 'infusion-pump' (Appendix 1). A few days were required for the ducks to regain their balance and to become accustomed to diving again with the 'dummy-packs'. Once trained, the left brachial artery of each duck was cannulated with PE 50 tubing under local anaesthesia (2% Xylocaine, Astra Pharmaceuticals, Toronto, CDN). The tip of the cannula was advanced to lie at the base of the aorta. The cannula was led, subcutaneously, from its point of insertion in the artery along the wing and over the clavicle to exit at a point in the midline of the back. The position of the catheter in the artery was verified by X-ray angiography. The cannula was flushed twice a day with heparinized saline (50 USP units ml'1 Heparin, Glaxo Canada, Toronto, CDN). An ECG transmitter (FM-1100-E3, Narco Scientific Ltd, Downsview, Ont) was implanted, under local anaesthesia, in the peritoneal cavity. The bipolar loop electrodes from the transmitter were positioned ventrally so that they lay at the base and apex of the heart. The transmitter was held in position within the peritoneal cavity with surgical silk. The peritoneal layer and abdominal walls were individually closed with surgical silk. The surgery sites were cleaned and swabbed, pre- and post- incision, with 10% povidone-iodine (Betadine, Purdue Fredrick Ltd, Toronto, CDN). Following surgery, each duck was given an 125 mg injection of ampicillin (Penbritin, Ayerst Laboratories, 30 Montreal, PQ) and allowed 1 to 2 days to recover before being put back on the diving tank. After recovery, the 'dummy-pack' was replaced by a flash-activated infusion pump. Blood flow distribution was measured under three conditions: rest, forced submergence, and unrestrained voluntary submergence. The rest condition was when ducks were unrestrained and sitting motionless. For forced submergence, the ducks were gently but firmly held while their heads were submerged in a beaker of water. Finally, for unrestrained voluntary submergence, the duck was left to dive on its own accord. Only one duck was used for voluntary blood flow distribution. The pump chamber of the infusion-pump pack was filled with 1 ml 9 9 mTc labelled macroaggregated albumin (MAA). Approximately 3 s after the start of a voluntary dive, the pump was triggered by an electronic flash. The infusion pump discharged at a rate of 30 mkmin"1. After the dive the duck was captured and a few millilitres of blood was withdrawn from the cannula to remove any residual 9 9 mTc. The infusion-pump was removed and the duck was scanned for the distribution of 9 9 mTc labelled MAA. The same injection system was used in the rest and forced submergence conditions, although MAA was injected approximately 10 s after the start of the forced dive. Scans for each experimental condition were done approximately 2 days apart. The voluntary dive was recorded with a stereo videotape system (Cannon Ltd, JPN). The telemetered electrocardiogram (ECG) signal was received through a FM receiver (Narco Bio Systems, Downsview, ONT), and was recorded on one of the audio tracks of the video tape. The video was later analyzed for the precise time course of events and calculation of heart rate. 31 R E S U L T S The relative blood flow distribution under three separate conditions as determined by injection of Q9mTc labelled MAA is presented in figure 2.1. Blood flow during rest was widely distributed throughout the duck's body (figure 2.1a&b). MAA injected approximately 10 s after the start of a forced dive, showed that blood flow distribution was concentrated in the chest and head regions while it was reduced in all other areas (figure 2.1c). These results are similar to those obtained from dabbling ducks (cf. chapter 1). However, in the case of the voluntarily diving duck injected 3.5 s after the start of a 7.2 s voluntary dive, blood flow distribution to the active leg muscles increased dramatically (figure 2. Id). This is particularly obvious when leg blood flow (figure 2. Id) is compared with the flow to leg muscles in both resting and forced dive states (figures 2.1a,b,& c). The pre-dive heart rate for the voluntary dive was 500 beats'min"1; the initial cardiac interval after submersion gave a heart rate of 187.5 beats'min"1; and during the 2 s infusion period heart rate was 181 beats'min"1. Immediately after surfacing, heart rate returned to 500 beats'min'1. 32 Figure 2.1 Gamma scans of ducks during rest, forced submergence and voluntary diving injected with 9 9 mTc MAA. a) rest - lateral view, b) rest - posterior view, c) forced dive - lateral view, d) voluntary dive - posterior view. 33 - REST LATERAL VIEW - FORCED DIVE 34 DISCUSSION The single result observation of blood flow during a volunatary dive confirms the suggestion, initially proposed by Eliassen (1960), that blood flow is maintained to active leg muscles in ducks during voluntary diving. Furthermore, blood flow distribution in diving ducks during forced submergence is similar to that found in dabbling ducks (Heieis and Jones, 1987). Interestingly, the pattern of blood flow distribution approximately 10 s after the start of a forced dive in diving ducks was the same as the distribution after 2 min of forced submersion in dabbling ducks (cf. chapter 1). This suggests that all of the cardiovascular changes in diving ducks occur much more rapidly than in dabbling ducks. The heart rate change observed during the voluntary dive is similar to those obtained by Furilla and Jones (1985) for Aythya americana during voluntary dives. This implies that the cardiovascular adjustments during the dive were relative^ unaffected by cannulation of the brachial artery. The greatest difficulty in attempting to collect data from free ranging ducks is interference with their natural behaviour. Lesser Scaup were found to train well and also to tolerate wearing backpacks for extended periods of time. In contrast, Redheads {Aythya americana) fitted with backpacks were never successfully trained and would sit and starve rather than dive into the water to eat. Obviously, the technical difficulties in obtaining blood flow distribution during voluntary diving in ducks can be overcome by judicious selection of the species and methodology. 35 Chapter 3 THE BIOENERGETICS OF SURFACE AND SUBSURFACE SWIMMING IN DIVING DUCKS (Aythya affinis) INTRODUCTION In their natural habitat, ducks dive for only a fraction of the time they are capable of surviving during forced laboratory dives (Eliassen, 1960; Woakes and Butler, 1983; Stephenson et al.,1986; Jones and Furilla, 1987). One significant difference between the two diving situations is that during voluntary diving ducks are actively using their leg muscles, whereas, during forced dives ducks are encouraged to be quiescent. There is presently only one estimate of oxygen consumption of ducks during voluntary diving (Woakes & Butler, 1983). Important as this finding is, a knowledge of the energy needed to dive is still required to fully understand the bioenergetics and limits of voluntary diving. Prange & Schmidt-Nielsen (1970) estimated aerobic efficiencies over a range of surface swimming velocities by measuring the oxygen consumption and surface drag force of ducks. Their values of surface drag, however, may be in error, as they merely used a hunters' decoy. Although Eliassen (1960) measured subsurface drag in stuffed guillemots, he used velocities above those observed in nature. So presently, for diving birds, there are still no reliable data available for the mechanical cost of diving. The object of this study was to estimate the mechanical cost of diving and to compare that cost with the cost of swimming on the water suface. The mechanical 36 power output of surface swimming was estimated from measurements of drag forces acting on ducks being towed in a water tank. However, when swimming close to or on the surface there is an additional drag force due to wave drag generated by the animal. This wave drag component decreases as the distance from the surface increases, and is reduced to zero when the diving depth is over 3X the body depth of the animal below the water surface (Hertel, 1966). Therefore, subsurface drag was also measured. Subsurface power output was determined from the measured subsurface drag forces and the buoyancy of live ducks. 37 METHODS Juvenile and adult Lesser Scaup (Aythya affinis) ranging in body mass from 0.40 to 0.75 kg were used in this study. Ducks caught in the wild were kept in an outdoor tank (4.16 m long, 1.87 m wide, & 0.65 m deep) located within the departmental animal compound. Ascent time was measured on 11 ducks that were manually submerged to a depth of 0.65 m and then released. Each duck was released in the position they normally assume on ascent from a voluntary dive. Times for only passive ascents were used for analysis; in other words, whenever a duck made attempts to actively swim, the data was discarded. The body volume of 12 ducks was determined by measuring the amount of water they displaced when submerged. (a) Buoyancy Measurements. Buoyancy was measured on 11 live Scaup. To measure buoyancy, the ducks were wrapped in a nylon body stocking and then strapped onto a harness with velcro straps. The harness was attached to the transducer by a fine nylon line. Ducks were completely submerged except for their beaks so that they could continue to breathe. The sinking force of the harness was measured and added to the recorded buoyancy values. Measured "gram force" (kg) was converted to Newtons (N) by multipling data by the gravitational acceleration of 9.8 nvs . A previously waterproofed force transducer, fFT03C, Grass Instruments, Quincy, MA, USA) was placed at the bottom of a fresh water tank at a depth of 0.5 m. A pressure-processor amplifier (model 13-4615-52, Gould, Cleveland, OH, USA) was 38 used to activate the transducer and amplify the output signal. Data from the pressure processor was collected for 5 min at 25 hz with an analog to digital (a/d) converter (DT2801-A, Data Translation, Marlboro, MA, USA) and stored on a computer (M24, Olivetti, Ivera, Italy) for later analysis. The output signal was also monitored on a storage oscilliscope (5113, Tektronics, Beaverton, OR, USA). The transducer was calibrated in the water with weights of known mass suspended via a pulley (lubricated to minimize friction) above the tank. The buoyancy of four floats was also measured, and these were used periodically to check the calibration of the transducer. (b) Surface & Subsurface Drag Measurements. Drag force was measured on frozen adult Scaup positioned either into their natural surface swirnrning position (n = 2) for surface drag measurements or in an extended "diving" position for subsurface drag measurements (n=5). Before freezing, metal bars were placed longitudinally and laterally within the ducks' body to ensure that the carcus maintained its shape and rigidity. Also, an aluminum post, used to attach the duck to the force transducer, was placed through the midline of the duck's back. Posts for surface measurements were approximately 10 cm long whereas posts for subsurface measurements were 35 cm long, 2.5 cm wide and 0.35 cm thick and were tapered on both the leading and trailing edges. The ducks were frozen in a deep freeze (-18°C) and were kept in an ice cooler filled with dry ice when being transported to the tow tank facility. For both studies, the legs were amputated above the knee so only body drag was measured. The drag force of the bars used for the subsurface drag studies were also measured and subtracted from the total subsurface drag measurements at each velocity range. Drag measurements were made approximately every 0.1 nrs'1 from 0.1 to 0.8 nrs"1 for surface and to 1.0 nvs"1 for subsurface drag measurements. Drag measurements were carried out on a tow tank located at the B.C. 39 Research Ocean Engineering Centre. The tow tank is equipped with a lightweight, manned, instrumented carriage. A computer (LSI 11/23, ADV-11 a/d board, Digital Equipment Corp, Marlboro, MA, USA) mounted on the carriage was used to collect and process data from a load cell (Model RUSB #200, Hottinger Baldwin Measurements, Framingham, MA, USA) to which a duck was attached by means of the aluminum post. The load cell was calibrated before measurements by suspending weights of known mass from it. An adjustable mechanical arm, to which the load cell was attached, was positioned so that for surface drag measurements, the ducks had the same water line as live ducks floating quietly on water. For subsurface measurements, ducks were held approximately 30 cm below the surface of the water. The tow tank dimensions were approximately 67 X 3.7 X 2.4 metres (length, width, & depth respectively). The carriage velocity was driven and controlled by a hydraulic system. The maximum velocity of the carriage was 4.5 nvs"1. (c) Statistics. Simple linear regression was used to determine the relation between mass and dependent variables. Analysis of variance for linear regression was used to test for significance (F < 0.01). The regression equations used were y = mx + b ± standard error of the estimate (SEE). Descriptive statistics used were mean ± standard deviation (SD). In some cases the range is given in parenthesis. Student's paired t-test was used to determine statistical significance (P < 0.01) between paired data sets. 40 RESULTS (1) Buoyancy and Body Volume. Mean ascent time for ducks manually released from the bottom of the tank was 0.826±0.286 (0.44-1.538) s (n = 69) yielding a mean ascent velocity of 0.787 nrs"3. The minimum ascent rate was 0.423 nrs"1 while the maximum was 1.477 m's"1. Buoyancy varied greatly between ducks and within individual ducks, depending on the phase of respiration (figure 3.1, table 3.1). The mean buoyancy at the begining of the trials was 0.953 ± 0.221 (0.686-1.47) N. Except for one duck in which buoyancy did not change, buoyancy declined at various rates over the 5 minute measurement period to a mean of 0.734 ± 0.214 (0.568-1.274) N. The decline in buoyancy between 0 and 300 s was statistically significant, and was not due to escape of air trapped in either the duck's feathers or harness. The average maximum peak force on inhalation measured at time 0 s was 1.047 ± 0.233 N, while the average minimum peak buoyant force on exhalation, including the baseline decrease of buoyancy, was 0.642 ± 0.207 N. Tidal volume remained relatively stable from the start to the end of each measurement period. The difference between the starting tidal volume of 17.8 ± 4.29 ml and value of 15.35 ± 4.45 ml after 5 min was not significant. There was no linear relation between body mass and buoyancy either at the beginning or end of each trial. Body volume was found to be linearly related to body mass (figure 3.2). The lowest bod}7 volume was 590 ml for a 424 g duck while the largest was 1000 ml for a 747 g duck. 41 (2) Surface and Subsurface Drag Measurements. Measured surface drag force increased slightly from 0.007 to 0.094 N between swimming velocities of 0.1 nrs"1 and 0.5 nrs"1 (figure 3.3a). However, at 0.5 m*s"\ the drag force increased sharply and reached 0.723 N at 0.8 nrs"1, which was approximately a 100X increase from the measured drag force at 0.1 nrs"1. Subsurface drag of ducks was obtained by subtracting measured bar drag from the total measured subsurface drag (figure 3.3b). The lowest corrected subsurface drag value was 0.042 N at 0.2 nrs"1, which was 0.024 N greater than surface drag at the same velocity. The subsurface drag force values increased almost linear]}- to 1.067 N at 1.0 nrs"1. That is a 25X increase from the value measured at 0.2 m's"1. 42 Figure 3.1 Buoyant force trace of a duck. The large spikes were struggles by the duck. 43 Table 3.1 Buoyancy and voluae values for 11 ducks. Buoyancy Tidal Voluae Resp Rate DUCK eass voluae 0 300 0 300 0 300 (g) ii) (N) (N) (Bl) (al) 10 414 0.620 0.941 0.647 12.600 14.800 30.000 30.000 8 424 0.590 0.725 0.470 16.800 12.600 18.000 21.000 3 502 0.765 1.029 0.813 12.700 8.100 40.000 35.000 12 512 0.670 1.000 0.647 23.300 13.400 24.000 36.000 11 522 0.730 1.009 0.755 13.200 15.900 24.000 27.000 9 547 0.690 0.686 0.686 15.200 15.200 33.000 30.000 7 588 0.860 1.470 1.274 22.700 21.300 27.000 21.000 2 595 O.BBO 0.931 0.755 18.500 20.500 34.000 33.000 5 600 0.810 0.764 0.568 20.600 10.800 30.000 38.000 6 602 0.850 0.970 0.725 22.400 20.900 30.000 30.000 1 747 1.000 0.882 19.100 40.000 es 530.6 0.747 0.953 0.734 17.800 15.350 29.000 30.1 44 Figure 3.2 Relationship between body mass and volume. 45 Figure 3.3a Surface drag of 2 frozen adult Lesser Scaup with both legs and feet amputated. Figure 3.3b Combined subsurface and bar drag (clear symbols). Bar drag (solid symbols). 46 Velocity (ms-') 47 DISCUSSION Results from this study support the basic assumption that swimming by ducks is energetically demanding, especially during diving. At low surface swimming velocities, drag remains relatively low until —0.5 nrs - 1 when it increases in an exponential fashion. In contrast, subsurface drag was higher at low swimming velocities, but at extremely high velocities, subsurface drag was less than surface drag. During diving, however, ducks have to work against drag during only the short descent period, but have to contend with buoyancy for all of the dive duration except for the ascent. The ascent velocity of 0.79 nrs" 1 was considerably higher than previous observations (0.55 m's'1, Butler and Woakes, 1982; 0.61 nrs" 1, Stephenson et al., 1986). These differences may be due to the deeper dive tanks used by prervious authors (1.55 m, Butler and Woakes, 1982; 1.7 m, Stephenson et al., 1986) and possibly behavioural changes in the ducks as a result of the constraints placed on them when diving (e.g. forcing the ducks to surface in one particular spot by covering the tank with netting). The most striking result of the buoyancy measurements was the decrease in buoyant force over time while tidal volume remained essentially unchanged. The decrease of buoyancy was most likely due to a reduction of functional residual capacity (FRC). That is, even though the average tidal volume remained the same, hydrostatic pressure may have forced air out of the air sacs. With each breath, therefore, ducks would exhale slightly more air than they inhaled. This is supported by the observation that when the ducks were taken out of the water, the harness straps, which had previously been snug, were very loose, indicating a reduction of body volume. Although body volume was related to body mass, this was not the case with buoyancy. The high variability between ducks could be due to any number of reasons, for instance 48 differences in plumage, muscle/body fat composition, or perhaps even stress which could have affected FRC at the start of the experiments. The surface drag measurements are lower than those previously reported (Prange and Schmidt-Nielsen, 1970). The difference is most likely due to the larger (1 kg) size of the duck models used by Prange & Schmidt-Nielsen (1970). It should be noted that in this study and that of Prange and Schmidt-Nielsen (1970) the drag of the propulsive system (i.e. legs and feet) was not measured. Therefore, any calculation of efficiencies based on these values will be underestimates, since any increase in drag will increase efficiency values. At swimming velocities below 0.5 nrs"1, the resultant drag force can be attributed mostly to the frictional interaction between the duck's wetted surface area and water. Above that velocity, however, surface drag increases almost exponentially with increases in swimming velocity. This increase is caused by surface wave interaction with the duck's body CHertel, 1963; Prange & Schmidt-Nielsen, 1970). Subsurface and surface drag are compared in figure 3.4. For the comparison, the surface drag curve was extrapolated from 0.8 nrs"1 to 1.0 m's"1 by means of a third order polynomial equation which was determined by a curve fitting program. These two curves cross over at approximately 0.78 nrs-1, so that at 1.0 m's"1, subsurface drag is 0.698 N less than the extrapolated surface drag value of 1.765 N. Therefore, the work required to overcome drag forces would be less for duck to dive rather than to swim at velocities at or above 0.78 nrs"1 (figure 3.4). Interestingly, horizontal subsurface swimming velocities for Aythya fuligula have been reported to be 0.89 nvs-1 (Stephenson, et al, 1986). 49 The higher drag force measured at low submerged swimming velocities occurs because the entire surface area of the duck is exposed to the water. As a result, larger frictional forces are generated as the duck moves through the water. Subsurface drag increased almost linearly because the wetted surface area remained constant and there was no added surface effect, since underwater drag was measured at greater than 3X body depth below the surface (Hertel, 1966). 50 2 Velocity (ms* 1) Figure 3.4 Surface and corrected subsurface drag forces. Surface drag was extrapolated from 0.8 nrs-1 to l'O nrs"1 for comparison. Ascent velocitj' for a duck with a buoyant force of 0.953 N would be approximately 0.95 nrs"1. With an ascent rate of 0.79 nrs-1 the resultant acting forces would be approximately 0.66 N. 51 General Discussion When ducks are forcibly submerged in water, they are faced with a life-threatening situation; that is, an increasely asphyxic state which may be continued for an unknown duration. Under such conditions, ducks make cardiovascular adjustments which are designed to prolong survival; they display a bradycardia, restrict blood flow to peripheral tissues, and as I have shown, mobilize their blood oxygen store to a central location where it is accessible to the two oxygen sensitive tissues; heart and brain. Since it has been shown that leg muscles lose their ability to function without a continued blood supply (Jones et al, 1987), and since I have also shown that the work required to dive is high (cf. chapter 3), it is proposed that in voluntarily diving ducks there are three oxygen dependent tissues, the heart, brain, and active leg muscles. It would be predicted from this Ivypothesis that blood flow will be maintained to these tissues during a voluntary dive. This was confirmed in the experiment described in chapter 2. Therefore, the main difference between the cardiovascular responses of forced and voluntary diving relates to the oxygen demand of the exercising muscle. The working leg muscles have been shown to be a significant drain on the oxygen stores as a result of their elevated metabolism and maintained blood flow during voluntas diving. I decided, therefore, to obtain a quatitative measure of the actual work and power output required to dive in order to assess the aerobic efficiency of voluntarily diving ducks. The "short" maximum dive durations observed in the wild associated with high oxygen consumption during diving (Eliassen, 1960; Woakes and Butler, 1983) suggest that diving is an energetically costly activity. Woakes and Butler (1983) estimated that oxygen consumption (i.e. power input) for unrestrained ducks diving to a depth of 1.55 m for an average duration.of 14.4s was 3.5X greater than at rest. 52 Therefore, given this data and those of the mechanical forces against which ducks have to work during diving, the amount of power required to dive can be calculated and hence, the aerobic efficiency be derived. This unitless value can then be used to compare the energetics of surface swimming with that of voluntary diving. To dive, ducks have to overcome two retarding forces. On descent, the duck has to work against buoyancy and the frictional forces incurred as it moves through the water (drag). Once the duck has reached the bottom of the tank, it needs to produce only enough power to counteract the force of buoyancy to remain there. On ascent, ducks do not actively swim but rise passively and therefore, use little energy in this latter phase of the dive. By definition, the amount of work done is equal to the product of the magnitude of the force and distance over which that force acts. In chapter 3, the forces acting against ducks as they dive were measured and the depth of the diving tank is also known, but when ducks are foraging at the bottom of a pond they are essentially stationary. Consequently, to calculate the work done against buoyancy during the foraging phase of a dive, a theoretical distance is calculated. It is assumed that when ducks forage at the bottom of a tank or pond, they do enough work to prevent themselves from surfacing, and are in effect swimming on a "tread mill". Therefore, the product of the ascent rate and duration of the foraging phase is the theoretical distance swam on the "tread-mill". The work done is therefore determined separately for each of the descent and foraging phases. Also, the observed values of dive duration and dive depth for voluntary dives by tufted ducks for which oxygen consumption was estimated (Woakes and Butler, 1983) will be used in the determination of work. The phase durations (descent, foraging, and ascent) of ducks diving to a depth of 1.55 m is determined by subtraction of both the descent and ascent times from the total dive 53 duration (14.4 s), given a descent rate of 0.57 nrs'1 (Butler and Woakes, 1979; Stephensen et al, 1986) and an ascent rate of 0.79 nrs"1 (chapter 3). The phase durations are 2.72 s for descent, 9.72 s for foraging and 1.96 s for ascent. Therefore, the distances travelled by the ducks would be 1.55 (depth of tank) for the descent phase and approximately 7.68 m (calculated assuming a "tread-mill" as described above) for the foraging phase. This foraging phase "distance", however, is likely to be a conservative estimate because there is a drag component which opposes buoyancy on ascent. The amount of drag encountered on ascent, which is a function of the ascent velocity, increases until the buoyant force equals drag force (figure 3.4). However, this is not a simple relation because air volume in the respiratory system probably expands during ascent, as hydrostatic pressure decreases causing a continued increase in buoyancy. The ducks therefore, probably accelerate during ascent. However, mean velocity was measured and is used here for calculations. Work done during a 14.4 s unrestrained dive: Decent Depth • Drag Force = 1.55 m * 0.35 N = 0.54 J Depth * Buoyancy = 1.55 m • 0.95 N = 1.48 J Work done during descent = 0.54 J + 1.48 J = 2.02 J Foraging Theoretical Distance * Buoyancy = 7.68 m * 0.953 N = 7.32 J Ascent = 0 Average Power Output during a 14.4 s unrestrained dive: Power Output = (2.02 J + 7.32 J) / 12.44 s = 0.751 W Power Output in 02 equivalent units = 0.751 W / 20 1 W'ml'Oj's'1 = 0.0374 ml 02 s"1 54 The average work done against a buoyancy force of 0.953 N during the descent and foraging phases is 1.48 J and 7.32 J respectively, and against drag forces of 0.35 N at 0.57 nrs"1 during the descent phase was 0.54 J. The average power output during dives is the total work done against drag and buoyancy divided by the period (12.44 s) over which it was done and is calculated to be 0.751 W. Therefore, if ducks were 100% efficient in converting their energy input into mechanical work, they would require an equivalent oxygen consumption rate of 0.0374 ml O^'s'1. Aerobic efficiency based on this power output (Po) value and the diving oxygen consumption (Pi) of 0.566 ml Og's"1 (Woakes and Butler, 1983) is 6.59% (Po/Pi * 100%). This is considerably higher than that obtained during maximal surface swimming (table GD.I), and also implies that ducks are much more efficient in utilizing their oxygen supply while diving as compared with surface swimming (--0.55 nrs'1) with the same level of oxygen consumption. During diving buoyancy is clearly the dominant force against which ducks have to work, while drag adds little ( — 6% of the total work required to dive) to the overall energetic demand. Therefore, any reduction in buoyancy will greatly reduce the energetic demands of diving. For instance, by exhaling tidal volume, ducks could reduce their work load to dive by —16%. In fact, studies by Butler and Woakes (1979) have shown that diving ducks submerge after exhalation. Therefore, a rerduction in respiratory volume prior to submersion may provide a mechanism by which the energy required to dive can be reduced by diving ducks. 55 TABLE GD.I Aerobic e f f i c i e n c i e s of surface sniaaing ducks. VELOCITY POWER INPUT Cvo2! POWER OUTPUT idrsgi EFFICIENCY (i/s) (Hi !N) (W) it) (1)* (2)** ! l i present (1) present (1) present rest 6.963 3.676 0.300 4.057 0.021 0,006 0.157 0.350 12.472 0.156 0.055 0,438 0.400 12.913 4.151 0.225 0.038 0.090 0.015 0.697 0.370 0.450 12.312 0.318 0.143 1.162 0.500 13.034 4.739 0.634 0.094 0.317 0.047 2.432 0.989 0.550 15.701 0.716 0.394 2.508 0.600 17.546 6.082 1.170 0.2U 0.702 0.126 4.001 2.076 0.650 19.751 1.180 0.767 3.863 0.700 23.280 8.068 1.560 0.413 1.092 0.289 4.691 3.579 0.750 0.800 12.192 0.723 0.578 4.744 * (1) Prance k Schaidt-Nielsen, 1970 ** (2) Data f r o * Woakes & Butler, 1983 and 1986 coabined 56 Appendix 1 Flash Activated Infusion Pump O Rings 1 \ [ | / D.C. Drive Motor Syringe Plunger S w j t c h CD 20 mm C1 R2 22 k C2 Zl\A R3 0.1 pt r - W V -7 8 IC 5S5 RESET R4 4.7k H v V v i R5 220 V+ S T I £ V W -R1 22 k to V-T1 - FPTWO T2-VN10KM(FET) 57 REFERENCES CITED Andersen, H.T. 1966. Physiological Adaptations in Diving Vertabrates. Physiol. Rev. 46,212-243 Blair, D.A. Glover, W.E., and Roddie., LC. 1961. Vasomotor Responses in the Human Arm During Leg Exercise. Circul. Res. 9,264-274 Butler, P.J. 1982. Respiratory and Cardiovascular Control During Diving in Birds and Mammals. J. exp. Biol. 100,195-221 Butler, P.J. and Woakes, A.J. 1979. Changes in Heart Rate an Respiratory Frequency Duirng Natural Behaviour of Ducks, with Particular Reference to Diving. J. exp. Biol. 79,283-300. Butler, P.J. and Woakes, A.J. 1982. Control of Heart Rate by Carotid Body Chemoreceptors during diving in Tufted Ducks. J. Appl. Physiol.:Resp. Environ. Exercise. Physiol. 53(6),1405-1410 Castellini, M.A., Murphy, B.J., Fedak, M., Ronald, K., Gofton, N., and Hochachka, P.W. 1985. Potentially Conflicting Metabolic Demands of Diving and Exercise in Seals. J. appl. Physiol. 58,392-399 Djojosugito, A.M., Folkow, B., and Yonce, L.R. 1969. Neurogenic Adjustments of Muscle Blood Flow, Cutaneous A-V Shunt Flow and Venous Tone During "Diving" in Ducks. Acta physiol. Scand. 75,377- 386 58 Guppy, M., Hill, R.D., Scheider, R.C, Qvist, J., Liggins, G.C, Zapol, W.M., and Hochachka, P.W. 1986. Microcomputer assisted metabolic studies of Voluntary Diving of Weddell Seals. Am. J. Physiol. 250 (Regulatory Integrative Comp. Physiol. 19) ,R175-R187 Eliassen, E. 1960. Cardiovascular Responsess to Submersion in Avian Divers. Arbok Univ. Bergen 2:1-100 Furilla, R.A. and Jones, D.R. 1985. The Contribution of Nasal Receptors to the Cardiac Response to Diving in Restrained and Unrestrained Redhead Ducks (Aythya americana). J. exp. Biol. 121,227-238 Heieis, M.R.A. and Jones, D.R. 1987. Blood Flow and Volume Distribution During Forced Sunmergnec in Pekin Ducks (Anas Platyrhynchos). Can. J. Zool. In Press. Hertel, H. 1966. Structure, Form and Movement. New York. Reinhold. Hudson, D.M. and Jones, D.R. 1986. The Influence of Body Mass on the Endurance to Restrained Submergence in the Pekin Duck. J. exp. Biol. 120,351-367 Irving, L., Scholander, P.F. and Grinnell, S.W. 1942. The regulation of Arterial Blood Pressure in the Seal During Diving. Am. J. Physiol. 135,557-566 Jones, D.R. and Holeton, G.F. 1972. Cardiac Output of Ducks During Diving. Comp. Biochem. Physiol. 4lA,639-645 Jones, D.R., Bryan, R.M., West, N.H., Lord, R.H., and Clark, B. 1979. Regional Distribution of Blood Flow During Diving in the Duck (Anas platy rhynchos). Can. J. Zool. 57,995-1002 59 Jones, D.R. and Furilla, R.A. 1987. In "Bird Respiration" Vol II. pages 75-125 C.R.C Press Boca Raton U.S.A. Jones, D.R., Furilla, R.A., Heieis,.M.R.A., Gabbott, G.R.J., and F.M. Smith. 1987. Forced and Voluntary diving in ducks: Cardiovascular adjustments and their control. Can. J. Zool. In Press. Kjellner, I. 1965. On the Competition Between Metabolic Vasodilation and Neurogenic Vasoconstriction in Skeletal Muscle. Acta, physiol. scand. 43,450-459 Langille, L. 1983. Role of Venoconstriction in the Cardiovascular Responses of Ducks to Head Emersion. Am. J. Physiol. 244 (Regulatory Integrative Comp. Physiol. 13) ,R292-R298 Murphy, B., Zapol, W.M., and Hochachka, P.W. 1980. Metabolic Activities of Heart, Lung, and Brain During Diving and Recovery in the Weddell Seal. J. appl. Physiol., Respirat. Environ. Exercise Physiol. 48,596-605 Millard, R.W., Johansen, K., and Milsom, W.K. 1973. Radiotelemetry of Cardiovacular Responses to Exercise and Diving Physiology in Penguins. Comp. Biochem. Physiol. 46A,227-240 Nickel, R., Schummer, A., Seiferle, E., and Wight, P.A.L. 1977. Anatomy of the Domestic Birds. Springer- Verlag, Berlin Prange, H.D. and Schmidt-Nielsen, K. 1970. The Metabolic Cost of swimming in Ducks. J. Exp. Biol. 53,763-777. 60 Qvist, J., Hill, R.D., Schneider, R.C, Fakle, K.J., Liggins, G.C, Guppy, M., Elliot, R.L., Hochachka, P.W., and Zapol, W.M. 1986. Hemoglobin concentrations and Blood Gas Tensions of Free Diving Weddell Seals. J. appl. Physiol. 61,1560-1569 Scholander, P.F. 1940. Experiments Investigated on the Respiratory Function in Diving Mammals and Birds. Hvalrad. Skirft. 22,1-131 Scholander, P.F., Irving, L. and Grinnell, S.W. 1942. Aerobic and Anaerobic Changes in Seal Muscles During Diving. J. Biol and Chem. 142,431-440 Stephenson, R., Butler, P.J. and Woakes, A.J. 1986. Diving Behaviour and Heart Rate in Tufted Ducks {Aythya fuligula). J. exp. Biol. 126,341-359 Taylor, C.R., Heglund, N.C, and Maloiy, G.M.O. 1982. Energetics and Mechanics of Terrestrial Locomotion. I. Metabolic Energy Consumption as a Function of Speed and Body Size in Birds and Mammals. J. exp. Biol. 97,1-21 Wiedeman, M.P. 1963. Dimensions of Blood Vessels from Distributing Artery to Collecting Vein. Circ. Res. 12,375-378 Woakes, A.J. and Butler, P.J. 1983. Swimming and Diving in Tufted Ducks (Aythya Fuligula), with Particular Reference to Heart Rate and Gas Exchange. J. exp. Biol. 107,311-329 Woakes, A.J. and Butler, P.J. 1986. 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