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The effect of oxygen and carbon dioxide on the diving behaviour and cardiac physiology of lesser scaup… Borg, Kim A. 2004

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T H E E F F E C T O F O X Y G E N A N D C A R B O N D I O X I D E O N T H E D I V I N G B E H A V I O U R A N D C A R D I A C P H Y S I O L O G Y O F L E S S E R S C A U P D U C K S (AYTHYA AFFINIS) by K i m A. Borg B. Sc., The University of British Columbia, 1999 A T H E S I S S U B M I T T E D IN P A R T I A L F U L F I L M E N T O F T H E R E Q U I R E M E N T S F O R T H E D E G R E E O F M A S T E R O F S C I E N C E in T H E F A C U L T Y O F G R A D U A T E S T U D I E S (Department of Zoology) We accept thisjfnesisVs conforn^ng^jthe required standard T H E U N I V E R S I T Y O F B R I T I S H C O L U M B I A May 2004 © K i m A. Borg, 2004 Library Authorization In presenting this thesis in partial fulfillment 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. Kim Bo^a If/OS /o*J-Name of Author (pleaseprint) Date (dd/mm/yyyy) Title of Thesis: ~~f[^ J tffysJ-'rj^L n^cjtto Asntl. <Lo^fa>^ jChjAAtoJ-frojC^ <s~£s It^f^ 5 ^ > ^ A(Jc-fiL<> (^Artjftitja/fi>TS*> Degree: /YICL&JTJ^- ^CS^ATU^. Y e a r : X£>OH Department of Io The University of British Colu Vancouver, B C Canada rrflDie^  Abstract The present study was designed to determine the relative influence of oxygen ( O 2 ) and carbon dioxide ( C O 2 ) on the cardiovascular and behavioral adjustments during voluntary diving in lesser scaup ducks. O f particular interest was how these animals allocate time during the dive cycle (travel time, foraging time and surface time) in response to various levels of inspired O 2 and C O 2 during short and long horizontal dives that are energetically more costly than vertical dives. Heart rate was monitored to determine the influence of peripheral chemoreceptors on cardiovascular control during voluntary dives as well as during dives when the animals were temporarily trapped underwater. Compared with normoxia, hyperoxia (50% O 2 ) exposure significantly increased dive duration in long dives, whereas severe hypoxia (9%) exposure significantly decreased dive time in both short and long dives. Hypercapnia (5%) had no effect on dive duration, but significantly increased surface interval duration. Mean dive heart rate during short dives (211.8 ± 6.9 beats min"1) was significantly higher than long dives (179.6 ± 5.0 beats min"1) although heart rate during all dives remained above resting levels. Heart rate during diving was unaffected in response to hyperoxia and hypercapnia during both short and long dives, but gradually declined in long dives after severe hypoxia exposure. A faster developing bradycardia to 90 beats min"1 at the end of short dives and to 70 beats min"1 at the end of long dives was evoked when the animals were trapped underwater. There were no significant differences in the response between trap dives after normoxia or hyperoxia. A model of oxygen store utilization during a voluntary dive quantified the critical Pao2 that necessitates cardiovascular adjustments in order to meet the metabolic needs of the tissues. During severe hypoxia, the critical Pao2 of 21 mmHg was reached 19 seconds into theoretical dives which corresponded with initiation of bradycardia in our severe hypoxia trials. The results suggest that O 2 and C O 2 levels in lesser scaup ducks are managed through changes in diving behavior without any major cardiovascular adjustments occurring throughout the dive. When the animals are pushed to the extremes of their endurance and Pao2 levels drop to threshold levels, a chemoreceptor induced bradycardia is evoked to conserve the remaining oxygen in the body. ii Table of Contents Abstract ii Table of Contents iii List of Tables iv List of Figures v Acknowledgements vi Chapter 1. The effect of O2 and CO2 on dive behaviour and cardiac physiology of lesser scaup ducks (Aythya affinis) Introduction 1 Dive behaviour 1 The effect of O2 and CO2 on dive behaviour 2 Cardiovascular responses during diving 3 Aerobic dive limit 5 Peripheral chemoreceptors in birds 6 Diving energetics 7 Purpose of this study 8 Materials and Methods 11 Dive tank setup and training protocol 11 Instrumentation 12 Experiments 13 Data analysis and statistics 15 Model of oxygen store utilization during a voluntary dive 19 Results 21 The effect of breathing various gas mixtures on dive behaviour :.21 The effect of dive distance on dive behaviour 22 Cardiac responses during short and long dives 23 Cardiac responses during exposure to various gas mixtures 24 Cardiac responses to trap dives 25 Discussion 26 Dive behaviour 26 Heart rate 30 Model of oxygen store utilization during a voluntary dive 33 Chapter 2. General discussion and conclusion 49 Freely diving lesser scaup ducks 51 Literature cited 54 List of Tables Table 1.1 Time allocation (seconds) of lesser scaup ducks during short and long dives following exposure to various gas mixtures 38 Table 1.2 Calculated swim speeds (m sec"1) of lesser scaup ducks during short and long dives following exposure to various gas mixtures 39 Table 1.3 Average heart rate (beats min'1) of lesser scaup ducks during short and long dives following exposure to various gas mixtures 41 Table 1.4 Average heart rate (beats min"1) of lesser scaup ducks during short and long trap dives following exposure to normoxia and hyperoxia 45 Table 1.5 Calculated oxygen storage capacity (ml O 2 kg"1) in lesser scaup ducks during exposure to various gas mixtures 46 iv List of Figures Fig. 1.1 Aerial view and dimensions of dive tank and apparatus 36 Fig. 1.2 Relationship between dive duration and surface interval duration during exposure to various gas mixtures 37 Fig. 1.3 Heart rate profiles (a) and averages (b) of short and long dives 40 Fig. 1.4 Heart rate profiles (a) and averages (b) of short dives during exposure to various gas mixtures 42 Fig. 1.5 Heart rate profiles (a) and averages (b) of long dives during exposure to various gas mixtures 43 Fig. 1.6 Heart rate profiles during short and long trap dives (a) and of long trap dives (b) following exposure to normoxia and hyperoxia 44 Fig. 1.7 Model of oxygen store utilization during a voluntary dive following normoxia exposure 47 Fig. 1.8 Model of oxygen store utilization during a voluntary dives following severe hypoxia exposure 48 v Acknowledgements First and foremost, I would like to thank my mom, dad, and sister for their support, motivation, and encouragement throughout this project. They've been with me through the ups and downs and I wouldn't have wanted to go through this without them. I am extremely grateful to Dr. David R. Jones for guiding me through this endeavor. I feel very lucky to have been a part of the 'Jones Lab' and to have learned from such an amazing physiologist. His assistance with surgeries, helpful input and uplifting personality made this a great experience. M y labmates Amanda Southwood, Nicole Elliott and Manuela Gardner have been very supportive over the years, and more importantly, have been great friends. I will never forget the infamous Dr.Pepper races and late nights at the Sugar Refinery. I'd also like to thank the boys, T. Todd Jones and Mervin Hastings, for providing comic relief in the office. They made the experience of writing this thesis more enjoyable. Manfred Enstipp has been a friend and mentor through the years. He has been a great resource for me and I thank him for all of his encouraging words, helpful edits, and his amazing perspective on life. I would also like to thank my committee members Dr. Bil l Milsom and Dr. Trish Schulte. Thanks to Bill for always taking time out of his busy schedule, for making me feel like part of the Milsom Lab, and for his efforts to make a physiologist out of me. Thanks to Trish for her valuable insight, encouragement, and advice. I thank all my friends and family who have always been there for me. In particular, my dear friends Erin Cebula, Satara Malloch, Madeleine Speck, Harley Kurata, Jan Ehses, and Andrew Pospisilik. I have learned so much from each of them. I would like to give a special thank you to Charles Darveau for his help and patience with developing the model in this thesis. More importantly, I'd like to thank him for his persistence and for being so grounding, supportive and for sharing this experience with me. Finally, I would like to dedicate this thesis to two very special people who passed away before it was complete. M y aunt, Doreen Parry, and my grandfather, Theodore Borg, who were, and always will be, my inspiration. vi Chapter 1 The effect of oxygen and carbon dioxide on dive behaviour and cardiac physiology of lesser scaup ducks {Ay thy a afjinis) Introduction Dive behaviour Diving birds that forage underwater are subject to various physiological constraints imposed by the environment that ultimately shape their diving behaviour. Most diving birds forage in bouts, performing a series of dives in quick succession interspersed with brief periods of time at the surface. While underwater, dive duration is influenced by their ability to manage finite oxygen (O2) stores and cope with the build up of carbon dioxide (CO2) and other metabolites. Between dives, the animals must readjust these variables to levels that are sufficient to enable another dive to occur. Presumably, natural selection will lead to optimizing dive behaviour so that net energy gained during the dive cycle is maximized. Avian divers that forage on sessile, benthic materials can accomplish this by maximizing the proportion of the dive cycle spent at the foraging site (Kramer, 1988). Several models have been generated to predict the foraging behaviour of diving animals. Kramer (1988) generated a hypothetical oxygen uptake curve representing the amount of oxygen taken up when an animal surfaces from a dive and starts breathing. The oxygen uptake curve could be used to predict the optimal amount of time an animal should spend at the surface replenishing its oxygen stores before performing another dive. In this model as dive depth increases, optimal surface time increases such that the proportion of the dive cycle spent underwater decreases. Building on Kramer's model, Houston and Carbone (1992) used the oxygen uptake curve to develop a model that 1 predicts the optimal amount of time to spend at the foraging site as well as at the surface in order to maximize energy gain for a particular dive depth. A unique feature of Houston and Carbone's analysis is that the optimal foraging time increases with travel time when travel time is short but when travel time is long, foraging time decreases. Both of these models are based on the premise that all dives are aerobic and that animals balance their oxygen gains and losses over a dive cycle. In other words, they assume that the oxygen level within the body is the proximate controller of dive behaviour. The effect of O2 and CO2 on dive behaviour The role of oxygen in determining time allocation during a dive cycle is unclear. Increasing the concentration of oxygen in the inspired air increases dive duration of redhead ducks (Furilla and Jones, 1986), but has no effect on tufted ducks (Butler and Stephenson, 1988). However, dive duration decreases in both of these species when exposed to hypoxic gas mixtures. The effect of oxygen on surface interval duration is equally contradictory. Halsey et al. (2003a) have shown that upon surfacing, tufted ducks fully reload their oxygen stores before another dive will commence, indicating that oxygen reloading influences surface interval duration. If exposed to hyperoxic gas mixtures, surface interval would be expected to decrease. This is the case in double-crested cormorants (Enstipp et al., 2001), but tufted ducks show no change in surface interval duration when exposed to hyperoxia (Butler and Stephenson, 1988). These studies further show that when exposed to hypoxic gases double-crested cormorants increase surface interval duration while tufted ducks reduce the surface interval. 2 Although these studies have conflicting findings, they reveal an important role for oxygen in shaping dive behaviour. Throughout a dive CO2 will accumulate in body stores potentially affecting dive behaviour. In response to hypercapnia tufted ducks decrease dive duration and surface interval duration (Butler and Stephenson, 1988) while double-crested cormorants show no change in dive duration, but the surface interval is increased (Enstipp et al., 2001). Recent work suggests that CO2 plays an important role in regulating surface interval duration. Boutilier et al. (2001) found that oxygen stores in gray seals were fully readjusted within three to four ventilations at the surface, but three to four more breaths were required to eliminate CO2 from the body before the next dive commenced. On the other hand, Halsey et al. (2003a) found, in tufted ducks, that accumulated CO2 was removed by the time O2 stores were fully replenished which makes the role of hypercapnia in prolonging surface interval contradictory. Halsey et al., (2003a) suggest that CO2 is more important in terminating dive duration than oxygen since tufted ducks exchange more CO2 than oxygen in the last few breaths before the first dive in a bout. Hence breathing high CO2 before a dive would be expected to significantly reduce dive duration, yet in cormorants it does not (Enstipp et al., 2001). These studies indicate that although both oxygen and CO2 affect dive behaviour, there is no universal agreement on the role of each on the behavioural components of a dive cycle. Cardiovascular responses during diving The physiological responses of air-breathing animals to submergence have been studied for over a century. Original experiments were conducted in a laboratory setting 3 where the animals were forcibly submerged for various periods. These studies determined that diving animals undergo a suite of physiological adjustments while underwater including apnea, bradycardia and peripheral vasoconstriction, causing an overall reduction in aerobic metabolism. These responses are collectively termed the 'diving response' and are believed to be a mechanism whereby oxygen is saved for anoxia intolerant tissues, namely the brain and heart, with the hypoperfused peripheral tissues resorting to anaerobic metabolism (Scholander, 1940). Advances in technology allowed for measurement of physiological variables on freely diving animals. These studies revealed that the responses to voluntary diving were less pronounced than during forced submergence (Millard et al., 1973; Butler and Woakes, 1979). In freely diving ducks, heart rate remains above resting levels during the dive (Butler and Woakes, 1979) and blood flow to the active leg muscles is maintained while flow to other regions such as the inactive wings and gut are reduced (Stephenson and Jones, 1992; Bevan and Butler, 1992). Furthermore, mean oxygen consumption during the dive is 3.5 times resting levels, similar to levels reached when the birds are swimming maximally on the water surface (Woakes and Butler, 1983). These, and other studies led to the proposal that voluntary diving in birds is a balance between exercise (increased blood flow to active muscles, increased oxygen consumption) and the typical oxygen conserving 'dive response' seen in forced submergence, with a bias towards the latter (Millard et al., 1973; Butler, 1982). Temporarily trapping lesser scaup ducks underwater during a voluntary dive causes abrupt changes in heart rate, which resemble the oxygen-conserving response seen during forced submergence (Furilla and Jones 1986). It has been suggested that the 4 bradycardia in these circumstances may be the result of dishabituation of the voluntary dive response back to the classic, forced dive response, causing a decrease in aerobic metabolism and thereby prolonging the period that the animal can stay underwater (Stephenson et al., 1986). Habituation occurs when a repeated stimulus produces a progressively weakened response. Therefore, with repeated exposure to submergence the classic dive response seen in forced dives may yield to a response more typical of voluntary diving (Gabbott and Jones, 1987). It has also been suggested that voluntary diving is conditioned on chemoreceptor input and that dishabituation, such as during trapping, will allow full chemoreceptor input to be expressed (Butler and Jones, 1997). Aerobic dive limit The aerobic dive limit ( A D L ) is the duration that an animal can sustain aerobic metabolism during a dive without resorting to significant increases in anaerobiosis (Kooyman et al., 1983). Direct measurement of the A D L via post-dive blood lactate levels, has only been performed on one species of diving bird, the emperor penguin (Ponganis et al., 1997) and revealed that the majority of dives performed by this species were within its A D L . Aerobic dives are favorable because lengthy surface intervals spent removing the by-products of anaerobic metabolism can be avoided. This allows the animal to maintain a high dive:pause (D:P) ratio, so that a series of aerobic dives can occur in rapid succession, leading to a maximization of underwater time. The A D L can be calculated (cADL) from the amount of oxygen stored in the body and the rate at which the store is utilized. Measurements of total body oxygen stores (Keijer et al., 1982; Stephenson et al., 1989) and diving metabolic rate (Woakes and 5 Butler, 1983; Stephenson, 1994; Halsey et al., 2003b) in tufted ducks indicate that the c A D L is much longer than their average dive duration in the wild. Certainly, the majority of dives performed by birds in the wild are assumed to be metabolically aerobic (Butler and Jones, 1997). Peripheral chemoreceptors in birds O 2 and C O 2 levels in arterial blood are monitored by carotid body chemoreceptors. These specialized regions in the vasculature are composed of glomus cells (Type I cells), sustentacular cells (Type II cells), and nerve terminals (Jones and Milsom, 1983). Sensory nerve discharges increase in frequency in response to decreasing arterial partial pressure of oxygen (Pac-2), increasing arterial partial pressure of C O 2 (Pacc-2) and decreasing pH. Conversely, discharge frequency decreases when oxygen tension is high, Paco2 is low or when arterial blood is alkaline (Acker, 1989). While there is a main consensus that partial pressure of oxygen is the stimulus for peripheral chemoreceptors, arterial oxygen content has also been suggested as an appropriate stimulus (Milsom, 1997) although there have been no measurements of the effect of arterial oxygen content on chemoreceptor output in birds. Peripheral chemoreceptor stimulation is an important regulator of ventilation (Bouverot and Leitner, 1972), but the level of Pao2 or Paco2 that causes change in ventilation varies between species (Faraci, 1986). During diving, when ventilation is not an option, the carotid body activation is expressed on the cardiovascular system (Jones and Milsom, 1983). Several studies have revealed the importance of chemoreceptor contribution to the cardiac responses to forced diving (Lillo and Jones, 1982; Mangalam 6 and Jones, 1984). For example, in Pekin ducks, peripheral chemoreceptors are responsible for 85% of the total forced diving bradycardia (Jones et al., 1982) While peripheral chemoreceptors play a major role in cardiovascular responses to forced diving, their role in voluntary diving is less clear. Butler and Stephenson (1988) found that denervating the peripheral chemoreceptors in tufted ducks elevates heart rate at the end of extended voluntary dives, suggesting that they play an important role in cardiovascular regulation at the latter portion of a dive. However, in their experiments, the birds swam horizontally (11 m) to the food and after foraging at a depth of 3m, rapidly decreased their depth and swam back to the surface at this shallow depth. Enstipp et al. (2001) have shown that double-crested cormorants have a greater cardiac response during shallow dives compared with deep dives of similar duration. They suggest that compression hyperoxia, an increase in Pao2 that occurs during descent to depth, delays chemoreceptor stimulation in deep dives so that heart rate remains higher than during shallow diving. Therefore, it is unclear whether the bradycardia observed in Butler and Stephenson's experiments is due to the rapid change in hydrostatic pressure experienced by the tufted ducks mid-dive that causes a reduction in Pao2, thereby stimulating the peripheral chemoreceptors. Diving energetics Most of the physiological studies on diving ducks conducted in a lab setting consist of short duration dives, similar to that seen in the wild when the animals are diving vertically for their food (Butler and Woakes, 1979; Parkes et al., 2002; Halsey et al., 2003a,b). During a dive, birds must overcome three forces; buoyancy, drag and 7 inertial forces of acceleration. When diving vertically, buoyancy contributes to 62% of the overall mechanical costs whereas drag comprises 27% and inertia 11% (Stephenson, 1994). During the foraging phase, when the animal remains stationary at the bottom, the contribution of these forces change to 87% for buoyancy and 13% for drag while inertial forces drop to zero. During the ascent phase, the animal passively floats to the surface and thus the energetic costs during this phase of the dive are very low. Therefore, energetic costs are affected by the durations of the behavioural phases of the dive (travel time and foraging time). Increasing the energy expenditure during diving might be expected to accentuate physiological changes (such as heart rate, Pao2, Paco2) that occur in a normal dive. Therefore, pushing animals to their physiological limits by increasing the energetic demands of the entire dive and increasing dive duration may lead to insights on the physiological mechanisms underlying diving behaviour. Purpose of this study The present study was designed to determine the relative influence of O2 and CO2 on the cardiovascular and behavioural adjustments during voluntary dives in lesser scaup ducks. In particular, I was interested in how these animals allocate time during the dive cycle (travel time, foraging time and surface time) in response to various levels of inspired oxygen and CO2 during short and long horizontal dives that are likely more energetically costly than vertical dives. Heart rate, measured by telemetry, was used as an indication of the role of peripheral chemoreceptors in regulating the cardiovascular system during these dives. Furthermore, I was interested in investigating whether or not 8 the cardiac response during trap dives is a result of dishabituation of the voluntary dive response allowing for expression of peripheral chemorecptor input. Because increasing the energetic costs of diving may shed light on the physiological mechanisms involved during submergence, I trained the animals to dive in a shallow tank so that they had to swim horizontally both to and from the food. The birds were trained to dive for short durations, similar to that seen in the wild, as well as for extended durations. The shallow tank eliminated any effect that depth may have on the cardiovascular responses to submergence. To investigate the role of peripheral chemoreceptors on cardiac responses to diving, the animals were exposed to various gas mixtures that have been shown to affect Pao 2 and Paco2 levels in birds (Mangalam and Jones, 1984). The gases were administered before diving as a means to enhance (via assumed decreased Pao 2 or increased Paco2) or silence (via assumed increased Pao2 or decreased Paco2) chemoreceptor input. This thesis tests four central hypotheses: 1) Dive duration is dictated by oxygen levels in the body and the effects of breathing altered oxygen levels before a dive will be expressed through changes in foraging duration, but not travel duration. 2) Surface intervals are dictated by CO2 levels in the body and the effects of breathing increased C 0 2 before a dive will extend surface interval duration. 3) Peripheral chemoreceptors do not play a role in cardiovascular regulation during short dives, but induce a gradual bradycardia during long dives. 9 4) The profound bradycardia evoked during trap dives represents dishabituation of the voluntary dive response allowing for expression of peripheral chemoreceptor input. 1 0 Materials and Methods Three adult female and three adult male lesser scaup ducks, Aythya affinis, with a mean mass of 660 ± 90g (mean ± S.D., range 582 - 738g) were used for all experiments. The animals were raised from eggs at the South Campus Animal Care Facility at the University of British Columbia (UBC) and subsequently housed there on a shallow diving tank for the duration of the study. A l l procedures in these experiments were approved by the U B C Animal Care Committee. Dive Tank Setup and Training Protocol Experiments were conducted using a shallow, flow-through freshwater tank (9m long, 0.60m wide, 0.55m high; Fig. 1.1) located in a covered outdoor enclosure where the animals were exposed to daily and seasonal fluctuations in daylight and ambient temperatures. The surface of the tank was covered with wire mesh so that the birds were restricted to surfacing at one end of the tank. The surfacing area and adjacent dry land area were enclosed by a wire cage, forming a holding area (1.9m length, 0.70m wide, 0.63m high). To encourage diving activity, a constant quantity of grain was added to discrete areas in the tank on a daily basis. Consequently, the birds were required to dive horizontally to and from the food. Dive duration could be manipulated and the energetic demands of the dive increased by altering the distance between the holding area and the food source. Furthermore, the shallow tank was used in order to eliminate any affect that depth may have on heart rate during diving (Enstipp et al., 2001). To obtain dive durations similar to that seen in the wild ('short dives', approximately 18-20 seconds in 11 duration), the food was positioned about 3.6m from the holding area (position Fs in Fig. 1.1). Following completion of the short dive trials, the birds were trained to extend their dive durations by gradually moving the food farther back in the tank until they were diving to the end, 9m from the holding area ('long dives', approximately 30 seconds in duration; position F L in Fig. 1.1). Trap dives consisted of temporarily denying access back to the surface during the return journey of a voluntary dive. For these trials, a weighted piece of plywood was suspended above the first corner of the tank (Fig. 1.1). The behaviour of the animals was monitored on a T V screen and the trap door could be lowered and raised remotely to block the passageway back to the dive enclosure. Instrumentation Heart rate data were collected by radio telemetry. Each animal was implanted with a small F M radio transmitter (T4D Medical Telemetry Implant, Konigsberg Instruments Inc., Pasadena, California, U S A ) while under isoflurane anesthesia. The transmitter (3 x 1 x 1cm) was interfaced with two electrocardiogram ( E C G ) leads. A small incision was made in the lower abdomen below the rib cage, and the body of the transmitter was positioned subcutaneously and sutured in place. Two small incisions through the abdominal muscles were made posterior to the ribcage and the two E C G leads were tunneled under the ribcage for placement on either side of the heart. The antenna of the transmitter was tunneled subcutaneously in the ventral thoracic region. The base of each lead was then sutured in place to surrounding abdominal muscles to hold it in place. Boroform antibiotic spray was administered to the suture areas before the skin incision was closed. Baytril antibiotic (2.5-5mg/kg) was administered 12 intramuscularly twice daily for three days and by that time the birds were behaving and eating normally and were therefore determined to have recovered from surgery. Heart rate recordings were not made until one week post-surgery. Each implanted transmitter was factory set to a specific radio frequency. To pick up the F M E C G signal from the birds, a custom made 300 Ohm twin lead antenna with four folded dipoles was designed and installed in the tank which allowed for E C G detection wherever the bird was in the tank or holding area. The antenna was wired into a two-channel telemetry receiver and demodulator (TR8-2-2/TD13, Konigsberg Instruments Inc., Pasadena, California, U S A ) , which allowed for tuning to two separate frequencies at a time. The E C G signal was viewed on an oscilloscope and recorded on the audio portion of V H S tapes. Concurrently, four video cameras were used to monitor the behaviour of the animals within the tank and this information was recorded on the video portion of the tape, thus allowing matching of diving behaviour with heart rate. A l l of the equipment was situated in a room adjacent to the tank to avoid disturbances to the animals during trials. Experiments Heart rate was recorded during short, long, and trap dives with the animals breathing various concentrations of gases before and after a dive. Experiments were run from November 2001 through to May 2003 during non-molting periods and water temperature was kept between 8-12 °C. Transparent vapor-proof polyethylene plastic was used to seal the holding area and medical grade gases (100% N 2 , O2, or CO2) were introduced at opposite ends of the 13 box until the desired gas concentration was achieved. Gas samples from the enclosure were passed through an O2 analyzer (S-3A/1, Applied Electrochemistry, Ametek Inc., Pittsburgh, Pa, U S A ) and a CO2 analyzer (CD-3A Applied Electrochemistry, Ametek Inc., Pittsburgh, P A , U S A ) . Two fans located at opposite ends of the holding area were left on for the entire duration of the experiment to ensure mixing and even distribution of gases. Throughout the duration of the trial, gases were sampled from directly above where the birds were diving and surfacing to ensure that gas for analysis was similar to that being breathed. Compressed air was continuously passed into the holding area when trials with other gases were not being run serving as a control and to allow the birds to acclimate to any noise generated by gas flow. A l l birds received the following gas treatments on separate days, in randomized order: i) Normoxia, (20.90% 0 2 , 0.03% C 0 2 ) ii) Hyperoxia (>50% 0 2 , 0.03% C 0 2 ) iii) Moderate hypoxia (long dives only; 13% O2, 0.03% CO2) iv) Severe hypoxia (9% O2, 0.03% C 0 2 ) v) Hypercapnia (20.90% 0 2 , 5% C 0 2 ) . These levels of gases were selected because they have been shown to affect diving heart rate in tufted ducks (Butler and Stephenson, 1988). At least five minutes were allowed before recordings were started to ensure that the animals' blood gases had equilibrated with the gases in the dive box. Experiments lasted between 4-6 hours and were conducted during daylight hours. Trap dives were performed during the normoxia and hyperoxia gas trials. When a bird swam past the trap to the foraging site, the trap door was lowered and kept in place for six to eight seconds and subsequently lifted to allow the bird to return to the enclosure to surface. Because the response to trap dives is subject to habituation (Stephenson, pers com) each bird was trapped only twice for both short and long dives. 14 Data Analysis and Statistics Dive behaviour Video tapes of diving behaviour were reviewed. For each gas treatment, all dives to the foraging site were analyzed for the following behavioural components: total dive time, travel time to the food, time spent at the foraging site (foraging time), and travel time from the food. A total of 930 short dives and 476 long dives were analyzed. The behavioural dive components were averaged for each individual animal and these values were compiled to generate a grand mean ± S E M (N = 6). One animal did not complete any dives to the food in the long dive 9% hypoxia treatment, therefore, all behavioural components in this treatment consist of five animals. Surface intervals were analyzed by determining the time spent at the surface between two consecutive foraging dives for all gas treatments. A l l surface intervals were compiled for each animal in each gas treatment and bout-ending analysis (Slater and Lester, 1982) was used to determine the cutoff point for a dive bout for each individual animal. Surface intervals greater than this value were excluded from analysis while shorter intervals were averaged to generate individual surface interval means. These animal means were then compiled to generate grand means ± S E M (N = 6) for all short and long dive gas treatments. Dive:Pause (D:P) ratios were calculated by dividing individual dive duration by subsequent surface interval duration for each bird in all treatments. Proportion of the dive cycle spent foraging (P forage) was calculated for individual birds using the equation: 15 P forage = foraging time foraging time + total travel time + surface interval Dive duration and surface interval duration means for individual animals were plotted for short and long dives to illustrate trends between the two variables. Data for normoxia treatments were normally distributed whereas the remaining three treatments were not normally distributed. Therefore, statistical analysis was not performed, but trend-lines were added for illustrative purposes. Swim speed was calculated by dividing dive distance (3.6m for short dives versus 9m for long dives) by travel time when swimming to and from the food. One-way repeated measures analysis of variance ( A N O V A ) was used to test between gas treatments within each behavioural component (dive time, travel time, etc.) for short and long dives. Student-Newman-Keuls multiple comparison was used as a post-hoc test. When single comparisons were made, as in differences between short and long dives within a gas treatment, Student's paired /-test was used. Significance was accepted at P<0.05. Heart rate Video tapes of dive behaviour and heart rate were reviewed and a total of six short and six long foraging dives were selected for each animal during exposure to each gas treatment. Dives were only selected form the third, fourth or fifth dives within a diving bout as pre-dive heart rate is most stable during this phase (Furilla and Jones, 1987). The electrocardiogram (ECG) from the selected dive was extracted from the video by running the audio portion of the video into Labtech Notebook Software (version 9.0, 16 Laboratory Technologies Corporation, Wilmington, M A , U S A ) . Instantaneous heart rate was computed by calculating the R - R intervals of the E C G using Acknowledge Software (version 3.01, B I O P A C Systems, Inc., Santa Barbara, C A , U S A ) , which were converted into beats min"1. Heart rate profiles were generated for short and long dives by analyzing heart rate 10 seconds before the dive (pre-dive), throughout the dive and 12 seconds following the dive (post-dive). Instantaneous heart rates were calculated and then averaged over 2 second time bins. For short dive gas treatments, only dives between 20-22 seconds in duration were analyzed. Dives that were longer than 20 seconds (i.e.: 21-22 seconds) were standardized to 20 seconds by removing individual R - R data points from the 18-20 second time bin of the instantaneous heart rate trace. For long dive gas treatments, only dives 30-32 seconds in duration were selected. To standardize the dives to 30 seconds, and heart rate from the 28-30 time bin was removed from the dives that were longer than 30 seconds. Long dive durations were shorter for both hypoxia treatments so they were standardized to a mean dive time of 26 seconds for mild hypoxia (13%) and 24 seconds for severe hypoxia (9%). For each bird, a total of six dives per gas treatment were analyzed to generate an average response for that animal. The animal means were then compiled to generate grand means ± S E M (N = 6). During trap dives, markers were made on the E C G recording when the animal apparently became aware of the trap door (indicated by a change in swimming behaviour) and when the trap door was lifted because previous experiments have shown that these behaviours coincide with a change in heart rate (Stephenson et al., 1986). Heart rate profiles were then generated for trap dives. Short dives (N = 6) were standardized to 20 17 seconds, including a 6 second trap and long dives (N = 4) were standardized to 36 seconds, including an 8 second trap. Each animal was trapped twice in normoxia and twice in hyperoxia. To generate heart rate averages for the various dive components, R-R intervals were averaged over the duration of the particular dive component (10 seconds for pre-dive, 20 seconds for short dive, 30 seconds for long dives, 10 seconds for post-dive, etc.). For trap dives, heart rate was also averaged over the trapping period, which started at the point the animal was aware of the trap door to the point when the trap door was lifted. Change in heart rate during the trapping period was determined by calculating heart rate during the last two seconds before the animal was aware of the trap door and subtracting the heart rate during the last two seconds before the trap door was lifted. To obtain resting heart rate, video tapes were reviewed for periods when the animals were quietly floating on the water surface, not interacting with any other birds or preening. Heart rate was averaged over the resting period for each animal in each gas treatment and then compiled as grand means ± S E M (N = 6). Comparisons between gas treatments of individual 2-second means of heart rate profiles (short and long dives) and of the dive component averages (pre-dive, dive and post-dive) were made using one-way repeated measures analysis of variance ( A N O V A ) with Student-Newman-Keuls multiple comparison tests. Comparison of heart rate averages between short and long dives within each gas treatment and heart rate between normoxia and hyperoxia for traps after short and long dives were made using Student's paired Mest. Significance was accepted at P<0.05. 18 Model of oxygen store utilization during a voluntary dive A model of oxygen utilization in the lung and blood during a voluntary dive was developed to determine the Pao2 level that initiates a chemoreceptor-induced bradycardia. The estimated oxygen storage capacities (ml O2 kg"1) in the lung (CLo 2) and blood of dive trained lesser scaup ducks were taken from Stephenson et al. (1989). Using the assumptions stated in that paper, as well as the oxygen-hemoglobin dissociation curve for duck blood (Scheipers et al., 1975), oxygen stores were recalculated for each of the oxygen concentrations used in my experiments (9%, 13%, 21%, and 50% oxygen). The small oxygen store in the muscle (5% of total oxygen store in normoxia) was not included in the model. Oxygen content in the lung (CLo 2) was assumed to be accessible for gas exchange during a dive (Boggs et al., 2002). Oxygen was removed from the starting CL02 in 0.93ml steps. The initial partial pressure of oxygen in the lung (PLo2) was set at 105 mmHg to account for hyperventilation before the dive. PLo 2 was calculated by multiplying initial PLcfc by the quotient of CLo 2 as a proportion of the original starting value. Arterial Po 2 (Pao2) values were calculated as PLo 2 -5 mm H g allowing for a constant diffusion resistance across the lung (Jones and Holeton, 1972). The saturation of hemoglobin at each Pao2 was obtained from the oxygen-hemoglobin dissociation curve. Arterial oxygen content (Cao2) is the product of arterial saturation and the oxygen carrying capacity of the blood (20.8 ml O2 100 ml' 1 blood; Stephenson et al., 1989). The metabolic rate (V02) was assumed to be constant throughout the dive. A range of metabolic rates reported in the literature were used in the model (Vo2 = 0.53, 0.93, or 1.46 ml kg' 1 sec'1; taken form Bevan et al., 1992; Woakes and Butler, 1983; 19 Stephenson et al., 1994 respectively), cardiac output ( Q ) was calculated using the Fick equation: Q = V02 and held constant throughout the dive. (Cao2- CV02) Q and Cao2 were multiplied to determine the proportion of oxygen lost from the arterial oxygen store. The value of arterial blood not passing through the tissues (total arterial blood volume - Q ) was multiplied by the arterial oxygen content of the previous cycle. These two values were added together to determine the arterial oxygen store. The content of oxygen in venous blood ( C V 0 2 ) was determined by subtracting the oxygen extracted from the arterial blood multiplied by venous blood volume. The venous store was corrected to account for the amount of blood passing through the tissues in one second as described above for the arterial store. The corrected venous and arterial stores plus the lung store were added to yield the corrected total oxygen store. The amount o f oxygen used after each step was calculated by subtracting total oxygen stores from the total of the previous iteration. This volume was divided by V02 to give time required to consume the oxygen. The time values were summed over the iteration to calculate the actual dive time that corresponded to each step of the iteration. The above sequence of calculations was repeated until the venous oxygen content dropped to zero. After this point, arterial oxygen content was insufficient to supply enough oxygen for the metabolic needs of the tissues without cardiovascular adjustment. The Pao2 when venous oxygen content fell to zero was therefore used as a measure of the critical Pac-2; the Pao2 that necessitated Q to increase oxygen supply or decrease to invoke the oxygen sparing diving response. 20 Results The effect of breathing various gas mixtures on dive behaviour The relationship between dive time and surface interval during exposure to the various gas treatments is shown in Figure 1 . 2 . For each treatment, an increase in dive time caused an increase in surface interval with hypercapnia and hypoxia ( 9 % ) showing a more dramatic increase than normoxia and hyperoxia. Short dives Compared with control (normoxia) animals, the only gas treatment that had a significant effect on short dive duration was hypoxia (Table 1 . 1 ) . The decreased dive duration during these treatments was due a decrease in time swimming to and especially from the food source (Table 1 . 1 ) . The animals also increased swimming speeds on the outgoing journey to food during hypercapnia treatments (Table 1 . 2 ) , but this did not cause a reduction in overall dive duration. Although the animals adjusted their swim speed during hypoxia and hypercapnia, time spent at the foraging site was similar to controls in short dives. Swim speeds were higher on the return journey from the food during all gas treatments (Table 1 . 2 ) . The largest effect on surface interval duration during short dives was hypercapnia exposure, causing a 1 1 5 % increase from controls. This increase in surface interval reduced the D : P ratio by 5 6 % . Surface intervals during hypoxia exposure were longer than controls, although the difference was not significant. Together with the decreased dive duration this caused a 5 6 % reduction in the D : P ratio compared with controls. The proportion of the dive cycle spent foraging (Pforage) was similar in all treatments. 2 1 Long dives Oxygen treatments had a significant effect on long dive duration whereas hypercapnia had none (Table 1.1). Breathing hyperoxic gas mixtures significantly increased long dive duration due to an increase in travel time as well as increased time spent at the foraging site. Hypoxia treatments significantly decreased dive duration, solely due to decreased foraging time. Foraging time during the mild hypoxia treatment (13%) was intermediate between the normoxia and severe hypoxia (9%) treatments. Swim speeds remained constant in all dives with the exception of hyperoxia (Table 1.2). Although hypercapnia had no significant affect on behavioural components of the dive, surface intervals were twice as long as control values, causing a significant decrease in the D:P ratio. Surface intervals were also higher than controls during 9% hypoxia exposure, but this difference was not significant due to the large variation in these surface intervals. The proportion of the dive cycle spent foraging was significantly lower than controls during hypercapnia and hypoxia exposure. During all gas treatments, excluding hyperoxia, the animals swam faster on the return journey from the food compared with travel speed to the food and these speeds were similar in each treatment (Table 1.2). The effect of dive distance on dive behaviour The 2.5 fold increase in distance to the long dive foraging site induced marked changes in dive behaviour (Table 1.1). Dive durations did not increase in proportion with dive distance because the animals swam faster during long dives (Table 1.2). Surface intervals within each gas treatment were significantly longer than the corresponding short 22 dive. The exception was during hypoxia treatments, which were longer, but not significantly due to large variation in long dive surface intervals. Long dive foraging time during normoxia, hyperoxia and hypercapnia treatments were similar to the corresponding short dive values. However, when exposed to low oxygen levels, long dive foraging time significantly decreased when compared to the corresponding short dive. Cardiac responses during short and long dives Comparisons of short and long dive heart rate profiles are illustrated in Fig. 1.3a and the corresponding heart rate averages for the dive components are given in Fig 1.3b and Table 1.3. Before the onset of a short dive, heart rate gradually increased reaching peak values of 3 5 3 . 5 ± 1 8 . 8 beats min"1 in the last two seconds before the dive (Fig. 1.3a). Upon submergence, heart rate dropped to an initial low of 1 7 7 . 5 ± 8 . 0 beats min"1 in the first two seconds of the dive, and increased to stable levels through the mid-portion of the dive. In the last six seconds before surfacing, there was a slight anticipatory increase in heart rate, which corresponded to the behavioural components of traveling from the food back to the surface. Upon surfacing, heart rate reached a peak of 3 7 4 . 9 ± 0 . 7 5 0 beats min"1 within the first four seconds post-dive and subsequently decreased with time spent at the surface. Heart rate profiles during long dives reveal similar pre- and post-dive heart rate patterns as short dives. However, during long dives heart rate progressively declined and dropped below short dive values by 14 seconds into the dive (Fig. 1.3a). The average diving heart rate during long dives was significantly lower than in short dives although 23 neither of these dropped below resting levels (Fig. 1.3b; Table 1.3). As during short dives, heart rate at the end of long dives slightly increased before surfacing. Post-dive recovery heart rates were significantly lower than in short dives. Cardiac responses during exposure to various gas mixtures Exposure to various gas mixtures during short dives did not have large effects on pre-dive or dive heart rates (Fig 1.4; Table 1.3). During hyperoxic exposure, pre-dive heart rates were lower than all other gas treatments, but the difference was not significant (Table 1.3). Diving heart rate was similar between all treatments although controls were highest and hypercapnic animals had the lowest diving heart rate values. After the dive, heart rates during all gas treatments were lower than controls with hyperoxic and hypercapnic animals being significantly lower (Table 1.3). Heart rate profiles show that these differences in post-dive heart rate occurred within the first two to six seconds after surfacing (Fig. 1.4a). Although there were no significant differences in average diving heart rates during long dives (Table 1.3), the heart rate profiles indicate that during hypoxia exposure (9%), there was a gradual decline in heart rate throughout the dive eventually falling below resting heart rates (Fig. 1.5a). Heart rate dropped significantly below control levels by 18 seconds into the dive reaching a minimum of 107.9 ± 7.0 beats min"1 by the end of the dive. It is interesting to note that the intermediate hypoxia treatment (13%) did not induce any cardiovascular changes from controls. After surfacing from hypoxia 9% dives, the peak in post dive heart rate was delayed by 4-6 seconds compared with controls. 24 Cardiac responses during trap dives During both short and long dives, when the birds became aware that they were trapped underwater, heart rate rapidly decreased below resting levels (Fig 1.6a). When the trap was lifted, heart rate slightly increased during the swim back to the surface and after surfacing, heart rate reached maximum post-dive values within 4-8 seconds. When trapped during short dives, heart rate dropped from average dive values by 59%, reaching 1 1 7 . 1 ± 1 4 . 8 beats min"1 during the first two seconds into the trap (Fig. 1.6a). Heart rate progressively dropped throughout the duration of the trap, reaching minimum levels of 9 3 . 7 ± 1 2 . 3 beats min"1. Trapping during long dives induced similar heart rate patterns as short dives, although average heart rate was slightly lower at the start of the trap and it reached minimum values of 6 8 . 3 ± 4 . 1 beats min"1 at the end of the trap (Fig. 1.6a). Although heart rate reached lower levels during long dive trapping, the relative change in heart rate between short and long trap dives were the same, both decreasing by approximately 100 beats min' 1 (Table 1.4). Pre-dive heart rate was lower than controls in hyperoxic animals although this difference was not significant (Fig 1.6b). During the dive, heart rate remained similar to controls and post-dive heart rate was significantly lower than controls due to a decrease in the last 10-12 seconds after surfacing. 25 Discussion Dive behaviour When the animals were exposed to elevated oxygen levels, there was no change in dive behaviour in short dives although dive time was prolonged in long dives. Increasing the oxygen concentration of the inspired air to 50% increases the total body oxygen stores by nearly 80% (Table 1.5). Using an average diving metabolic rate for tufted ducks of 0.9 ml O2 sec"1 kg' 1 (estimated from values reported by Woakes and Butler, 1983 and Halsey et al., 2003b) the calculated aerobic dive limit ( cADL) during hyperoxic exposure is 84 seconds. Therefore the potential exists to extend aerobic dive duration beyond the 30 seconds that occurred in long dives, making it apparent that the animals in this study surface well before their oxygen stores are depleted. A disconnect between the size of the oxygen store and dive time in hyperoxia exposure has also been observed in tufted ducks as well as in double-crested cormorants (Butler and Stephenson, 1988; Enstipp et al., 2001 respectively) and is typical of the majority of dives performed by birds and mammals (Butler and Jones, 1997). A 'safety reserve' of oxygen stores left in the body is beneficial as these stores can be exploited i f the animal must remain underwater for extended periods of time, such as to avoid predators or if trapped underwater. In contrast to increasing oxygen stores in the body, decreasing oxygen had significant effects on both short and long dive behaviour. Durations of long distance dives during hypoxia exposure corresponded to the concentration of oxygen breathed before the dive (Table 1.1) with moderate hypoxia dive durations being intermediate between controls and severe hypoxia treatments. The c A D L for moderate hypoxia is 37 seconds and the animals surfaced well within this limit. Reducing the inspired oxygen 26 concentration to 9% causes a 41% reduction in total body oxygen stores (Table 1.5) thereby reducing the cADL to 28 seconds, which was well above short but close to long dive durations. Nevertheless, the birds responded by reducing durations of both short and long dives compared with controls. Behavioural observations during severe hypoxia treatments indicate that the animals were reaching the limits of their endurance. On occasion the birds were observed to switch from leg propulsion to wing propulsion, suggesting that the leg muscles were possibly anoxic and had lost their capacity for force generation (Jones et al., 1988). These results suggest that oxygen levels within the body dictate dive duration and that low oxygen levels are a strong stimulus to terminate a dive. Surface intervals following short and long dives for severe hypoxia treatments were longer than controls although due to the large variability in surface times, the differences were not significant. Following many of the 9% hypoxia dives, the birds would not perform another dive for a considerable duration yet the analyzed surface times are between two consecutive dives, an event that occurred infrequently. Therefore, it is likely that these surface intervals are underestimated. The above notwithstanding, long surface intervals are indicative of extra time being required to correct acid-base disturbances caused by anaerobic end products. In long dives the birds significantly increased swimming speed by 30% compared with that in short dives and in all dives the birds increased swimming speed on the return leg from the food. Lowest swimming speeds on both legs occurred after breathing hyperoxic gas. The swim speeds in the short dives were similar to those of tufted ducks diving vertically on a shallow tank (0.55 m sec"1 Woakes and Butler, 1983; 0.68 m sec"1 Loworn et al., 1991). An increased swimming speed implies a higher rate of oxygen 27 utilization due to the increase in mechanical costs of diving. Drag forces that occur with increases in underwater swim speed do not change substantially up to 0.5 m sec"1. Above this speed drag increases exponentially and reaches about 20% of the buoyant force at the highest speeds recorded in the present experiments (Stephenson, 1994). Consequently, the faster swim speeds during long dives compared to short dives will increase the metabolic costs of long dives. This seems contraindicated especially after exposure to moderate or severe hypoxia. It is difficult to decipher why the animals in this study increase swim speed during long dives rather than swim at slower speeds (presumably at the lowest cost of transport) and extend dive duration. These types of questions can't be addressed without knowing the energetic costs of locomotion during short and long horizontal dives. Alteration in long dive duration during exposure to low oxygen concentrations was due to decreases in foraging time as traveling time remained the same as controls. Foraging time seems to be relatively unchanged under a given set of conditions only falling when the ducks are pushed to extremes of their endurance (Butler and Stephenson, 1986). Certainly, endurance limits appeared to be reached during the severe hypoxia trials because the birds were reluctant to dive for their food and had to be fasted for several days to induce diving. Also, the birds did not reach the food during a large portion of dives and turned back to surface (these dives were not included in the analysis). Hypercapnia exposure had no effect on short or long dive durations. These results contrast with those of Butler and Stephenson (1988) who found that the dive duration of tufted ducks decreased during hypercapnia exposure. They suggest that the increased Paco2 during a dive is a strong stimulus to ventilate and is the signal that terminates a 28 dive. Halsey et al. (2003a) also suggest that hypercapnia is more important in asphyxia tolerance compared to hypoxia. In a study on rhinoceros auklets, Stephenson et al., (1992) have shown that Paco2 levels do not change during escape dives. Similarly, Paco2 of Weddell seals during 20 minute voluntary dives only increases by 10 mmHg (Qvist et al., 1986). Boutilier et al. (2001) suggest that Paco2 remains low during a dive because CO2 is stored in the tissues due to their high CO2 capacitance. Therefore, the high levels of CO2 in the hypercapnia treatments of the present study may be preferentially stored in the tissues during the dive where it would not alter PAco2 or Paco2- Regardless of where the CO2 is stored during a dive, it has no effect on dive duration of the animals in this study. CO2 clearance rates are slower than O2 uptake rates and dictates surface interval duration. CO2 must be mobilized from stores in the tissues and blood that build up during a dive (Boutilier et al., 2001). Thus, the more chemically complex mechanisms involved in C 0 2 removal during the surface interval compared with oxygen uptake will increase the time to readjust CO2 back to the pre-diving level. Gray seals remain at the surface until built-up C0 2 levels are readjusted even though oxygen stores are replenished within the first couple of breaths (Boutilier et al., 2001). On the other hand, CO2 in tufted ducks is readjusted to normal values about the same time as oxygen stores are restocked (Halsey et al., 2003a) suggesting that CO2 in ducks is more readily accessible than in gray seals. Certainly, it is acid-base imbalance that drives ventilation after forced dives because arterial blood gas levels of CO2 are restored long before ventilation returns to normal (Milsom et al., 1983). 29 The dive:pause ratio (D:P), an indication of diving efficiency, is highest during short normoxia and short hyperoxia dives. The D:P ratio is far lower in both short and long dives after exposure to severe hypoxia and hypercapnia. In the 13% hypoxia treatments, surface intervals were similar to controls and so were the D:P ratios. Due to the non-proportionate relation between dive and surface time the D:P ratio also declines between short and long dives under all imposed conditions. Therefore, the most efficient diving behaviour occurs when the animals perform short duration dives that necessitate short surface intervals. Heart rate The overall heart rate patterns in response to short horizontal dives in this study are similar to those of ducks performing short vertical dives (Butler and Woakes, 1979; Stephenson et al., 1986; Bevan and Butler, 1992; McPhail and Jones, 1998). During long dives, heart rate gradually declined below short dive heart rate levels by 14 seconds into the dive, but still remained well above resting levels (Fig. 1.3a). Heart rate in long dives was below that in short dives after 14s but only in normoxia was average heart rate significantly different between short and long dives (Fig. 1.3b; Table 1.3). Because heart rates were similar during hyperoxia, normoxia and moderate hypoxia, the reduction in heart rate cannot be attributed to chemoreceptor input. Although McPhail and Jones (1998) have shown that increases in energetic costs of diving have little influence on heart rate, a decrease in metabolic rate with increased dive duration has been observed in tufted ducks (Bevan et al., 1992) and is possibly due to a decrease in buoyancy through the dive as air is progressively lost from the feathers (Butler and Jones, 1997). In my 30 study, a trail of air bubbles was seen when the birds were diving and the resulting decrease in buoyancy could potentially affect heart rate and can account for the differences in heart rate seen in short and long dives. Heart rates during short or long dives were not influenced by the gases breathed pre-dive except 9% oxygen. In long dives the decline in heart rate with time was gradual but major and rapid changes in heart rate occurred 18 seconds into long dives following severe hypoxic exposure and heart rate continued to fall as the dive progressed. Heart rate fell below resting levels; a true diving bradycardia. Hence it seems unlikely that peripheral chemoreceptors play any significant role in dives unless Pac-2 declines below a threshold level which is obviously not reached in the majority of dives performed by this species. This conclusion is not new because Butler and Woakes (1982) showed that in short dives by tufted ducks carotid body denervation had little effect on diving heart rate except at the end of the dive when heart rate of denervates was significantly above that of intact birds. This was also the case in longer dives when heart rate fell (between 7.5 and 32.5 seconds of diving) almost twice as fast in intact and sham operated birds as in denervates (Butler and Stephenson, 1988). Shams and intact ducks achieved a true bradycardia while heart rate in denervates never fell below resting levels. Therefore, the bradycardia observed in their experiments was not likely due to changes in hydrostatic pressure as I suggested in the introduction. Because heart rate declined below rest by 25 seconds into the dives, it appears that, compared with our study, their birds had a higher metabolic rate and caused Pao2 to drop to threshold sooner. In contrast, a study in diving cormorants indicated an important role for chemoreceptors in control of heart rate 31 (Enstipp et al., 2001). Mean dive heart rate was significantly lower during shallow compared with deep diving, possibly due to an increase in Pao 2 during the descent phase of the dive (compression hyperoxia). As might be expected, exposure to hyperoxic and hypoxic gases before the dive increased and reduced mean dive heart rate in cormorants (Enstipp et al., 2001). Not all birds appear to be the same when it comes to cardiac control during voluntary diving. Although Pao2 was not directly measured in this study, Mangalam and Jones (1984) have shown that exposure of 50% oxygen increases Pao2 from 90 mmHg to 240 mmHg in Pekin ducks. Exposure to 12.8% oxygen reduced Pao2 to 70 mmHg. Therefore, the gas concentrations administered in this study are likely to have altered the blood gases in a similar way. Obtaining Pao 2 values from freely diving birds is difficult. Cannulation of the brachial artery has been shown to cause elevation in heart rate and would therefore, skew diving heart rate measurements (Woakes and Butler, 1986). Furthermore, handling time that is required to take blood samples imposes stress on the animals, which would likely alter their diving behaviour. On surfacing from a dive, heart rate returns to levels close to those established immediately pre-dive and then declines. Halsey et al. (2003a) showed that after short dives restoration of oxygen and CO2 stores was completed more or less simultaneously and usually before the next submergence. Heart rates are high in the post-dive period but even so circulation times will be on the order of 15s (Bevan & Butler, 1994) yet it appears that restoration of stores occurs within one circulation time. Given this, it is not surprising that the impact of slight but significant changes in post-dive heart rate had little influence on surface intervals in the present experiments. 32 The most rapid and largest declines in heart rate seen in the present experiments were induced by trapping birds under water. Again a major chemoreceptor contribution to the bradycardia does not appear to be present even though the sudden bradycardia resembles the oxygen-conserving response seen during forced dives (Jones & Purves 1972; Furilla and Jones 1986). In the present study, heart rate levels during trapping after short dives was higher than the levels reached after long dives, however, the rate of decline was similar in both (Fig. 1.6a). Also, the response after breathing hyperoxic gas pre-dive was the same as in ducks diving from normoxia. These observations were expected for although denervation of carotid bodies significantly slows the evolution of the cardiac response to trapping there is no effect on the initial sudden decline in heart rate in intact, sham-operated and denervated ducks (Butler & Stephenson, 1988). It is possible that the visual stimulus when the animals see that they are unable to surface initiates a fear type response, and that suprabulbar inputs override any other afferent inputs that are acting during the dive. Fedak (1986) reported that any 'surprising' stimulus during a voluntary dive induced a force dive heart rate response in gray seals. Similar responses are observed in muskrats when they escape from David Jones and are motionless underwater (McCulloch and Jones, 1990). Model of oxygen store utilization during a voluntary dive The present study indicates that peripheral chemoreceptors do not play a major role in heart rate control during voluntary dives of less than 30 seconds in lesser scaup ducks. However, during long dives after severe hypoxia treatments, a bradycardia was induced and indicates that chemoreceptors are active when oxygen levels drop to a 33 threshold level. It appears that the peripheral chemoreceptors are more sensitive to oxygen than C O 2 as hypercapnia had no effect on diving heart rate. Therefore, a model of oxygen store utilization in the lung and blood during a voluntary dive was used to determine the critical Pao2 that invokes expression of chemoreceptor-induced bradycardia. Fig. 1.7a and b illustrate the absolute and relative changes in oxygen stores of the lung and blood during a voluntary dive when the animals are consuming oxygen at a rate of 0.93 ml kg"1 sec"1 (see Materials and Methods for details). The large oxygen store in the lung serves as an oxygen reservoir 'topping up' arterial blood to maintain hemoglobin saturation, and thus content, at high levels. Thus, at the beginning of a dive, the lung oxygen store falls quickly whereas the rate of decline in the arterial store is slow (Fig. 1.7b). When Pao 2 declines to levels that cause large drops in saturation, the arterial store starts to decline more rapidly (about 15 seconds into the dive; Fig. 1.7) while the venous stores decline even faster. Approximately 35 seconds into the dive, arterial oxygen content drops to levels that are insufficient to supply aerobic metabolism in the tissues at the given metabolic rate. At this point, the animal must increase cardiac output to maintain aerobic metabolism, or switch to a heavier reliance on anaerobic metabolism and conserve the remaining oxygen for anoxia sensitive tissues. At this point in the dive total oxygen stores equal 7.0 ml kg"1 and, according to the calculations in the Materials and Methods, this oxygen store value corresponds to a Pao2 of 26 mmHg and is referred to as the critical Pao 2 (Fig. 1.7a). 34 Although it was not measured in my study, others have produced an estimate of the diving metabolic rate for tufted and lesser scaup ducks ranging from 0.53 to 1.46 O2 kg"1 sec"1 (Woakes and Butler, 1983; Bevan et al., 1992; Stephenson, 1994; Halsey et al., 2003b). From figure 1.7c one can estimate the dive times required to reach critical Pao2at these different metabolic rates during normoxia. The longest dives recorded during my normoxia treatments were 28 seconds during which no bradycardia was observed. Therefore, the diving metabolic rate of the birds in my study is not likely as high as 1.46 ml O2 kg"1 sec'1. When exposed to severe hypoxia, total oxygen stores are reduced by 46% with the largest decline occurring in the lung store. Fig. 1.8 (a and b) illustrate how the oxygen stores are utilized during an hypoxic dive. At the onset of the dive, due to the low oxygen store in the lung, arterial stores start to decline quickly and by 19 seconds the critical Pao2 of 21 mmHg is reached, corresponding to total store of 5.5 ml O2 kg"1. Switching to an oxygen conserving mode at this time in the dive will prolong the remaining oxygen stores for 30-60 seconds. During the hypoxia treatments in my study, a bradycardia occurred 18 seconds into the dive. This is consistent with the model prediction of bradycardia occurring at 19 seconds into the dive when metabolic rate is 0.93 ml O2 kg"1 sec"1 (Fig. 1.8c) and is likely a close approximation of the diving metabolic rate of the birds in my study. 35 3.6m Carbon dioxide analyzer Receiver / demodulator Fig. 1.1. Aerial view and dimensions of dive tank and apparatus. The shaded region in the holding area represents open water where the animals were diving and surfacing. The entire surface of the tank was covered with a wire mesh cover, which is not illustrated. Fs indicates location of food for short dives; F L indicates position of food for long dives. 36 Fig. 1.2. Relationship between dive duration and surface interval duration during exposure to various gas mixtures. Trendlines are for normoxia (solid line) hyperoxia (dash and dot) hypercapnia (long dash line) and hypoxia (dotted line) treatments. Data points represent individual animal means during short and long dives. N=6 for all gas treatments with the exception of long hypoxia dives where N=3. 37 "1 ^ Su D. 0s go *B O I* W 2 •a o o s "H o Eo-o e e © Q. s O w "es s. 3 #© « cu CQ •n o +1 00 * CS © -H r-VO * 4t Tt T t co © CO <n o\ © o © o • <n © ' © ' in o © -H -H -H © ' -H -H -H -H •n -H 00 00 o -H O in r-' © VO VO co i—4 •n Tt o © 4— * co # Tt <=> o•H .+! * O ©' O CN Tt-' -H oo CS ro o CS O © -H OS o © 00 ro r- 00 CS o © ©' ©' ©' cs ©' ©' +1 -H -H -H -H -H -H r- 00 CS ro cs ro os r-' s d >ri ©' cs © cs ro <n © © o -H -H -H i n M N •n « S cs rt -H cs ©' cs a o c -9 <2 9? 5 « g .SS 2 o £ _ t* 1 0 "3 -a g * S ? > > a C P — o & 2 .3 * © -H r-00 en Tt ©' -H cs T t CS • CS Tt * t> CS o o o Tt T t o -H -H o © o T t T t -H 41 -H -H o CS r- Tt o CS sd © eooi 4— 4— eooi ro © -H o s d cs cn cs * t> © ' © CS s d -H -H © -H o en -H r-cs © ' 00 Tt cn Tt o +1 so ©' * * * 00 in o o o +1 +1 +1 r- r~ o o cs cs en rH 4— 4— 4— * CO rt CS vd o o +1 -H -H 1/1 VO m vd in O vd •»— 4— * s o o -H Tt r--o o in 00 en CS vo o o o o O o CO Tt o -H •n o o +1 +1 -H O +1 o +1 -H r- r- r- +1 o -H rn r-' —4 o cn Tt r- r~ o cs •n Tt o o o 4— 4— 4— 4— o 1 a o c« Q H H U< P 3 -X w D s< a g £ o -fc 2 2 J Q H H o cs B (D ... i "° a « c on -a s •cl. CJ CM 2 <§ j i . H M D 2 > > a 0 0 '52 1 2 ^ 38 Table 1.2. Calculated swim speeds (m sec'1) of lesser scaup ducks during short and long dives while exposed to various gas mixtures. Behavioural component Normoxia (21% 0 2) Hyperoxia (>50% 0 2) Hypoxia (13% 0 2) Hypoxia (9%0 2) Hypercapnia (5% C 0 2 ) Short dives Travel to food 0.48 ± 0.01 0.46 ± 0.02 - 0.55 ±0.03 * 0.54 ±0.02 * Travel from food t 0.63 ± 0.03 0.59 ±0.03 - t 0.72 ± 0.00 * 0.61 ± 0.03 Long dives Travel to food 0.78 ± 0.02 % 0.71 ± 0.02 J * 0.75 ± 0.02 0.79 ± 0.02 J 0.76 ± 0.02 { Travel from food t 0.85 ± 0.02 % 0.76 ± 0.03 % * t 0.87 ± 0.02 t 0.87 ± 0.03 X t 0.82 ± 0.00 X Values are means ± SEM (N=6), measured in m sec •Significantly different from normoxia values within corresponding dive component (One way Anova; PO.05) J Significantly different from corresponding short dive component (Paired t-test; P<0.05) tSignificantly different from travel to food within the short or long dive component (Paired t-test;P<0.05) 39 500 400 Si 300 <D e3 200 E 100 Long dives Short dives t t -10 0 10 20 Time (sec) —i— 30 40 50 500 jr^ 400 CO 300 3 200 1 E 100 H 0 B Short dives Long dives pre-dive dive post-dive Figure 1.3. Heart rate profiles (A) of short and long dives performed by lesser scaup ducks. Heart rate profile values are means ± S E M averaged over two second intervals from six dives per bird. Bold arrows indicate point of submergence and surfacing, respectively. The horizontal dotted line represents average resting heart rate Heart rate averages (B) during the pre-, dive, and post-dives components. * Significantly different from short dive. 40 Table 1.3. Average heart rate (beats min ) of lesser scaup ducks during short and long dives while exposed to various gas mixtures. Dive Normoxia Hyperoxia Hypoxia Hypoxia Hypercapnia Component (>50%) (13%) (9%) (5%) Rest 129.7 ± 7 . 7 157.8 ± 9 . 4 138.2 ± 17.3 157.7 ± 17.8 164.3 ± 14.6 Short dives Pre-dive 323.9 ± 17.0 237.2 ± 17.7 - 297.6 ± 30.4 295.3 ±34 .5 Dive 211.8 ± 6 . 9 201.8 ± 9 . 8 - 197.8 ± 17.1 184.1 ±12 .7 Post-dive 330.2 ± 13.3 247.7 ± 1 5 . 9 * - 288.4 ± 26.2 266.1 ± 2 6 . 9 * Long dives Pre-dive 289.6 ± 17.6 258.8 ± 14.0 294.5 ±30 .5 300.8 ± 36.6 308.4 ±23 .8 Dive t 179.6 ± 5 . 0 1 8 5 . 6 ± 7 . 4 181.6 ±3 .3 157.2 ± 17.5 178.8 ± 7 . 4 Post-dive t 288.1 ± 16.9 240.2 ± 6 . 1 * 293.3 ± 9 . 7 250.2 ± 9 . 7 273.5 ± 11.2 Values are grand means (beats min") ± S E M (N=6) * Significandy different from normoxia values within corresponding dive component (One way A N O V A ; P<0.05) •f Significantly different from short dive values of corresponding dive component (Paired t-test; PO.05) 41 X ioo H -10 0 10 20 30 40 Time (sec) 500 - i pre-dive dive post-dive Figure 1.4. Heart rate profiles (A) of short dives performed by lesser scaup ducks during exposure to various gas mixtures. Heart rate profile values are means ± S E M averaged over two second intervals from six dives per bird. Bold arrows indicate point of submergence and surfacing, respectively. The horizontal dotted line represents average resting heart rate. The data were normalized so that dives of different lengths ended at the same time. Heart rate averages (B) during the pre-, dive, and post-dives components. + Hyperoxia, - hypercapnia, * hypoxia values significantly different from control (normoxia). 42 500 400 A % 300 13 200 100 n— -10 0 500 ^ 400 B Normoxia Hyperoxia Hypercapnia Hypoxia 9 % Hypoxia 13% t 10 20 Time (sec) 30 —I— 40 50 Normoxia Hyperoxia g | Hypoxia 9% H H Hypoxia 13% Hypercapnia pre-dive dive post-dive Figure 1.5. Heart rate profiles (A) of long dives performed by lesser scaup ducks during exposure to various gas mixtures. Heart rate profile values are means ± S E M averaged over two second intervals from six dives per bird. Arrows mark submergence and surfacing respectively. The horizontal dotted line represents average resting heart rate. The data were normalized so that dives of different lengths ended at the same time. Heart rate averages (B) during the pre-, dive, and post-dive components. * Significantly different from control (normoxia) values. 43 500 ~ P 400 300 <L> 200 X 100 0 t f Long dive trap Short dive trap ~i 1 1 1 1 1 1— -10 0 10 20 30 40 50 Time (sec) 500 ^ 400 A 0 B Normoxia Hyperoxia -10 0 I— 10 - n 20 —i— 30 40 50 60 Time (sec) Figure 1.6. Heart rate profiles during short and long trap dives (A) and of long trap dives while exposed to normoxia and hyperoxia (B). Bold arrows denote beginning and end of the respective dives. Arrow marked't' indicates point where animals were aware of the trap door, V indicates when the trap door was lifted. Heart rate profile values are means ± S E M averaged over two second intervals from two dives per bird for both short and long trap dives. N = 6 birds for short trap dives, N = 4 birds for long trap dives. Dotted horizontal line indicates resting heart rate. + Significantly different than corresponding trap dive heart rate during short dive. * Significantly different from control (normoxia) values. 44 Table 1.4. Average heart rate (beats min1) of lesser scaup ducks during short and long trap dives while exposed to normoxia and hyperoxia. Dive component Trap dive normoxia Trap dive hyperoxia (>50%) Short dives Pre-dive 271.5 ±32 .1 265.5 ±31 .8 Dive 197.0 ± 14.1 197.1 ± 18.2 Trap 105.6 ± 14.9 118.9 ± 17.8 Post-dive 323.7 ±22 .1 319.2 ± 15.4 M i n Trap 93.7 ± 12.3 90.3 ± 20.4 Change in trap HR 98.0 ± 10.8 101.1 ± 16.2 Long dives Pre-dive 285.0 ±35 .0 220.3 ± 28.6 Dive 188.0 ± 6 . 4 167.9 ± 13.1 Trap 76.6 ± 12.5 77.0 ± 7.6 Post-dive 312.4 ± 6 . 5 230.4 ± 14.0 * M i n Trap 68.3 ± 4 . 1 71.3 ±12 .9 Change in trap HR 99.3 ± 11.8 89.8 ± 10.5 Values are grand means (beats min"1) ± S E M (N=6 for short dives, N=4 for long dives) * Significantly different from normoxia value within corresponding dive component 45 Table 1.5. Calculated oxygen storage capacity (ml O2 kg'1) in lesser scaup ducks during exposure to various gas mixtures. Gas mixture Lung/air sac system Arterial blood Venous blood Muscle Total Normoxia (21% 0 2) 18.9 7.9 12.9 2.3 42.0 Hyperoxia (50% 0 2) 45.0 8.5 19.7 2.3 75.5 Hypoxia (13% 0 2) 11.7 7.2 11.7 2.3 32.9 Hypoxia (9% 0 2 ) 8.1 5.5 9.0 2.3 24.9 See Materials and Methods for calculations 46 B 100 2 c s I § ! I Total Lung Arterial Venous Critical Pac>2: 26 mmHg 10 15 20 25 30 35 40 Dive time (sec) 10 15 20 25 30 35 40 Dive time (sec) 0.93 ml O z kg"1 sec"1 0.53 ml O z kg"1 sec"1 1.46 ml 0 2 kg"1 sec-1 10 20 30 40 50 60 70 80 Dive time (sec) Fig. 1.7. Model of oxygen store utilization during a voluntary dive following normoxia exposure. A) Absolute changes in oxygen stores in the lung and blood during a dive using a V02 of 0.93 ml O2 kg"1 sec"1. Vertical dotted line represents the 'critical Pac*'. B) Relative changes in the oxygen stores as percent of starting values. C) Total oxygen store utilization at various V02 s. Horizontal line represents total oxygen store for critical Pace (from A). Vertical arrows indicate the dive time when the critical Paca is reached for each V02. 47 o-l , , , = — I 0 5 10 15 20 Dive time (sec) 0 5 10 15 20 Dive time (sec) C 0 10 20 30 40 50 Dive time (sec) Fig. 1.8. Model of oxygen store utilization during a voluntary dive following severe hypoxia (9%) exposure. A) Absolute changes in oxygen stores in the lung and blood during a hypothetical dive using a metabolic rate of 0.93 ml O 2 sec^kg*1. Vertical dotted line represents the 'critical Paca'. B) Relative changes in the oxygen stores as percent from starting values. C) Total oxygen store utilization at various V02 s. Horizontal line represents total oxygen store for critical Pao2 (from A). Vertical arrows indicate the dive time when the critical Pao2 is reached for each V02. 48 Chapter 2 General discussion and conclusion Altering inspired gas levels before voluntary diving provides valuable insights into mechanisms underlying the dive behavior and cardiac physiology of lesser scaup ducks. M y study indicates that during the majority of dives, O2 and CO2 levels in the body are managed through changes in diving behavior without any major cardiovascular adjustments occurring throughout the dive. Oxygen levels within the body primarily influence dive duration while CO2 is important in determining surface interval duration. Increasing the energetic costs of a dive by extending dive duration and increasing traveling costs accentuates the physiological responses that are typical of routine diving. When the animals are pushed to the extremes of their endurance, such as during long hypoxic dives or trapping, more profound cardiovascular adjustments are evoked. Based on the first hypothesis of my thesis, I predicted that altering inspired oxygen levels before a dive would alter dive duration mainly through changes in foraging time but not travel time. Furthermore, increasing inspired CO2 levels would have no effect on dive duration. While I found that high and low oxygen levels do indeed alter dive duration, the changes were mainly due to changes in travel time since foraging time remained relatively constant. It is only when the animals are nearing their endurance limits (hypoxia long dives) that foraging time was reduced. Increased CO2 levels had no effect on dive duration, indicating that oxygen levels in the body limit the duration of a voluntary dive. M y prediction based on the second hypothesis that surface interval duration would be longer after breathing C 0 2 before a dive whereas inspired oxygen levels would 49 not alter surface interval duration. This hypothesis was confirmed. I found that surface interval durations were extended in short and long dives after breathing high CO2. Altering oxygen levels had little effect on surface interval duration during short dives, in long severe hypoxia dives, when there was evidence of anaerobiosis, surface interval increased. Therefore, CO2 clearance sets surface interval duration during aerobic dives. For my third hypothesis, I predicted that heart rate during short dives would remain above resting levels, and that breathing different 0 2 or C 0 2 mixtures would have no effect on diving heart rate. During long dives, I predicted that a gradual decline in heart rate below resting levels would occur throughout the dive and breathing high oxygen (high Pao2) levels would mask the effect whereas low oxygen levels or high CO2 (low Pao2, high Paco2) would enhance the bradycardia. I found that in both short and long dives heart rate is above rest during the entire dive, indicating that peripheral chemoreceptors do not play a major role in heart rate responses during these dives. It is only when the animal is exposed to severe hypoxia during long dives that a bradycardia occurs. By developing a model of O2 store utilization, I was able to estimate the critical Pao2 that induces the bradycardia. This Pao 2 was 26 mmHg during normoxia exposure and 21 mmHg during severe hypoxia exposure. M y final hypothesis was that the profound bradycardia evoked during trap dives represents dishabituation of the voluntary dive response allowing for full expression of peripheral chemoreceptor input. I predicted that hyperoxia exposure before the dive would eliminate the bradycardia seen in trap dives. However, exposing the animals to high oxygen levels before the dive had no effect on the development of bradycardia during trapping, indicating that the cardiovascular responses to trapping are not a result of 50 dishabituation. Other factors such as input from facial receptors or visual cues are likely to play a role in the cardiac response to trapped dives. Freely diving lesser scaup ducks Wild lesser scaup ducks typically forage in open waters <3m deep and perform dives averaging 22 seconds long (Custer et al., 1996), feeding mainly on benthic invertebrates and vegetation (Austin et al., 1997). Optimal foraging models predict that in order to maximize net rate of energy gain over a dive cycle, foraging time should decrease when travel time is long (Houston and Carbone, 1992). However, my results show that foraging time remains the same in both short and long normoxia dives even though travel time was considerably different. This indicates that the birds in this study do not conform to the predictions of optimal foraging models. It is interesting that during short dives the animals do not spend longer at the foraging site. The cardiovascular responses during both short and long normoxia dives indicate that the animals are functioning within their aerobic capacities. The c A D L during normoxia is 43 seconds (using metabolic rate of 0.93 ml O2 kg' 1 sec'1; Woakes and Butler, 1983; Halsey et al., 2003b) and the animals surfaced well before this time in all dives. Therefore, the animals have the capacity to extend dive time while maintaining aerobic metabolism. Increasing foraging time would increase the net energy gain during the dive. However, longer dives require longer periods at the surface to recover such that extending dive time would decrease the D:P ratio. This may explain why the animals do not unduly increase short dives duration. 51 Foraging constraints may be an alternative explanation for why foraging duration remains constant in short and long dives although travel time changes. Foraging time in lesser scaup ducks increases compared with controls when food densities are low (Samantha Richman, pers comm). In my study, food was provided in excess and thus there were no limitations caused by low food density. Although Tufted ducks swallow underwater (de Leeuw et al., 1999) there is a maximal amount of food that lesser scaups ducks can manage though force-feeding (Samantha Richman, pers com). Therefore, foraging time in this study may simply be a reflection of the maximal amount of food that can be acquired during the dive. In experimental conditions when food is provided in excess, foraging time doesn't change until endurance limits are reached. Tufted ducks diving horizontally to foraging sites at various distances spend a similar amount of time foraging until they reach long distances (10m) after which foraging time decreases (Stephenson et al., 1986). Tufted ducks diving vertically to 2.2m or 5.5m depth spend the same amount of time at the foraging site even though dive duration increases (de Leeuw, 1996). Therefore, when food is provided in excess, it appears there is an upper limit to foraging duration in diving ducks which may be due to maximum quantity of food uptake. In the wild, food densities and food depth (depth under substratum) may have stronger effects on foraging time. The present study indicates that lesser scaup ducks perform well within their aerobic capabilities. Heart rate remains well above resting levels during short and long dives and the animals surface well before their calculated aerobic dive limit. Diving efficiency (D:P ratio) is highest when dive durations are short. Maintaining a high D:P ratio throughout a bout is beneficial for shallow divers as it allows the animals to perform 52 a series of dives that are within their aerobic capabilities without resorting to anaerobiosis. This is advantageous because accumulation of end products from anaerobic metabolism during a series of dives could potentially end a diving bout. For pursuit divers that must search and catch moving prey, there are situations where extending dive duration past the c A D L is profitable, such as when prey are difficult to locate and capture (Ydenderg and Clark, 1989). Pursuit divers such as the South Georgian Shag frequently perform dives that are longer than their estimated aerobic dive limit (Bevan et al., 1997) as do some species of penguin (Green et al., 2003). For these animals, economical usage of oxygen stores through employment of more severe oxygen conserving mechanisms will be beneficial during diving (Green at al., 2001; Green et al., 2003; Bevan et al., 1997). In conclusion, my study indicates that lesser scaup ducks meet their foarging needs by performing a series of short duration, shallow dives that are not accompanied by major cardiovascular adjustments. 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