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Bioenergetics in the killer whale, orcinus orca Kriete, Birgit 1994

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BIOENERGETICS IN THE KILLER WHALE, ORCINUS ORCAbyBIRGIT KRIETEB.Sc., Trent University, 1982Honours B.Sc. Trent University, 1983A THESIS SUBMITTED IN PARTIAL FULFILLMENT OFTHE REQUIREMENTS FOR THE DEGREE OFDOCTOR OF PHILOSOPHYinTHE FACULTY OF GRADUATE STUDIESDEPARTMENT OF ANIMAL SCIENCEWe accept this t s as conformingch,eiest •daTHE UNIVERSITY OF BRITISH COLUMBIAAugust 1995© Birgit Kriete, 1995In presenting this thesis in partial fulfilment of the requirements for an advanceddegree at the University of British Columbia, I agree that the library shall make itfreely available for reference and study. I further agree that permission for extensivecopying of this thesis for scholarly purposes may be granted by the head of mydepartment or by his or her representatives. It is understood that copying orpublication of this thesis for financial gain shall not be allowed without my writtenpermission.(Signature)Department of (i1ML gC?The University of British ColumbiaVancouver, CanadaDate OJJ i /95DE.6 (2/88)ABSTRACTA series of three papers is presented, each one related to the bioenergetics of killer whales,Orcinus orca. The first chapter describes how standard and realized metabolic rates weredetermined in captive killer whales by collecting respirations at different apneas and differentactivity states by training the animals to exhale into a funnel onto which a meteorologicalballoon was attached. These exhalations were analyzed for tidal volumes and respiratorygases; estimates of realized metabolic rates were based on activity budgets observed in theindividual animals. Tidal volumes at rest were 2.7 to 4.2 times higher than those predicted byallometric equations, while estimated vital capacities are estimated to lie between 68% and94% of the values predicted by allometric equations. Standard metabolic rates for the adultanimals were similar to Kleiber’s estimates (1.2 to 1.3 times Kleiber). Realized metabolicrates were between 2.7 and 2.9 times those of the whales’ SMR, which are values similar tothose of terrestrial mammals.In the second chapter, food consumption and the influence of other factors such aspregnancy, lactation and water temperature on the food intake of captive killer whales, wereexamined. Food data were collected from the aquaria at which the animals were held andanalyzed for caloric values on a daily basis. While food intake increased with age, differencesin water temperature ranging between 7 and 23 °C had little or no effect on food intake.Pregnancy caused an increase in food consumption of 25% only during the last month ofgestation, but food intake increased up to 100% with lactation. The best fit for feeding rateas a function of body weight was determined as: food intake (kg/d) = 0.277 M°663, where11M = body mass in kg. A mean net assimilation efficiency of 0.73 was calculated bycomparing food intake to energy expenditure measured by respiration analysis.In the third chapter, realized metabolic rates were estimated in free-ranging killer whalesalong the Pacific West Coast of British Columbia and Washington. Swimming velocities andrespiration rates were determined by tracking movements of whales using a theodolite and aloran. The relationship between swimming velocities and respiration rates showed an increasein respiration rate with increasing swimming speed for different age and sex classes of killerwhales. These data were combined with metabolic rates determined by respiration analysis incaptive killer whales during different activity states to estimate metabolic rates of wild killerwhales during swimming (males: metabolic rate (kcal/kg/d) = 29.32 + l.11V25; females:metabolic rate (kcal/kg/d) = 32.29 + l.26V25). The minimum cost of transport for male andfemale killer whales occurred at 3.1 rn/sec which corresponded to 0.18 and 0.20 kcal/kg/km.The drag that killer whales experience at different swimming velocities was calculated basedon theoretical assumptions and suggests that drag is mainly laminar (males: 88% of the flowwas laminar and 12% were turbulent; females: 89% of the flow was laminar and 11%turbulent).111TABLE OF CONTENTSAbstract.iiTable of Contents ivList of Tables viiList of Figures ixAcknowledgements xiDedication xiiiPreface xivChapter 1. METABOLIC RATES IN CAPTIVE KILLER WHALES, Orcinus orcaINTRODUCTION AND OBJECTIVES 1METHODS 7Study Animals 7Metabolic Rate Determination 7Respiration Rate Determination 8Daily Activity Budget Determination 9Collection of Expired Air 9Tidal Volumes, Oxygen and Carbon Dioxide Ratios 13Weight Estimates 16Standard Metabolic Rate Estimates 16Daily Energetic Expenditure 17Metabolic Scopes 18Respiratory Quotient 18RESULTS 19Respiration Rates 19Apnea and Tidal Volume 19Respiratory Gases 24Standard Metabolic Rates 31Activity Budgets and Estimated Daily Caloric Expenditures 36Metabolic Scopes 36Respiratory Quotients 36DISCUSSION 39Tidal Volumes and Respiratory Rates 39Apnea and Observed Rates of Oxygen Consumption 41Estimated Standard Metabolic Rates 44Estimated Daily Caloric Expenditures 46Metabolic Scope 474ivDifficulties and Reliability 48Chapter 2. FOOD CONSUMPTION AND THE INFLUENCE OF OTHER FACTORSON FOOD iNTAKE IN CAPTIVE KILLER WHALES, Orcinus orcaiNTRODUCTION AND OBJECTIVES 50METHODS 56Age Estimation 56Weight 58Food Data Collection 58Urine Collection and Net Assimilation Efficiency 61Growth 62Statistical Analysis 62Temporal Variation of Food Consumption 62Variation in Food Consumption between Individuals 62Water Temperature 63Reproductive Status 63Food Consumption Relative to Body Weight 63Determination of Net Assimilation Efficiency 64RESULTS 64Food Consumption and Individual Variation in Food Intake 64Factors Related to Variation in Food Intake 68Temporal Variation of Food intake within Individuals 68Water Temperature 68Reproductive Status 72Growth 72Food Consumption Relative to Body Weight 72Net Assimilation Efficiency and Daily Caloric Consumption Vs. Daily CaloricExpenditure 75DISCUSSION 77Food Intake and Individual Variation in Food Consumption 77Water Temperature 78Reproductive Status 79Comparison between Caloric Intake and Caloric Expenditure and NetAssimilation Efficiency 80Chapter 3. COST OF TRANSPORT, DRAG AND REALIZED METABOLIC RATEESTIMATES IN FREE-RANGING KILLER WHALES, Orcinus orca5VINTRODUCTION AND OBJECTIVES .81METHODS 87Swimming Speeds, Respiration Rates and Diving Depths 88Theodolite Study 88Southern and Northern Boat Study 91Analysis 92Track Distance Calculations 92Dive Models 93Swimming Velocities 95Cost of Transport 96Morphometrics 98Fineness Ratio 98Reynolds Number 98Drag 99RESULTS 101Observations 101Diving Depths and Dive Models 101Bias 102Breathing Rates and Swimming Velocities 102Metabolic Rates 107Cost of Transport 109Morphometrics 109Fineness Ratio 109Reynolds Number 112Drag 112DISCUSSION 112DiveModels 112Bias 114Respiration Rates, Swimming Velocities and Metabolic Rates 115Cost of Transport 115Fineness Ratio, Reynolds Numbers and Drag 117Estimated Daily Caloric Expenditure 119Chapter 4. SUIVllv1ARY AND CONCLUSIONS 120LITERATURE CITED 1266viLIST OF TABLESTable Page1. Summary of respiratory data from four captive killer whales 202. Two-way ANOVA to test for variation of tidal volume among individual whalesbetween Activity states 1 and 3 223. Differences in tidal volume for individual whales in different activity states 224. Significance of differences in tidal volumes between individual whales in the sameactivity state 235. Regression equations and statistics for the relationship between oxygen extraction andapnea and carbon dioxide production and apnea in four killer whales 296. Comparison of slopes of oxygen extraction as a function of apnea in different activitystates for two killer whales 307. Comparison between mean apnea and mean oxygen consumption and carbon dioxideproduction at mean tidal volumes for different activity states for four killer whales 328. Comparison between mean apnea and mean oxygen consumption and carbon dioxideproduction at maximum tidal volumes for different activity states for four killer whales 329. Mean oxygen extraction at mean apnea during different activity states for four killerwhales 3210 Estimates (kcallkg/d) for standard (SMR) and basal (BMR) metabolic rates for killerwhales 3511. Hourly caloric expenditure of four killer whales for different activity states 3812. Average number of hours spent in different activity states by four killer whales 3813. Daily energetic expenditure of four killer whales 3814. Metabolic scopes of four killer whales based on respiration rates and caloricexpenditures 387viiTable Page15. Description of the study animals and availability of food records 5716. Estimated weight of six killer whales based on their length 6017. Individual variation in food intake among six captive killer whales 6718. Temporal variation of food consumption by month and year for six captive killer whales .... 6919. Comparison between daily energetic expenditure measured by respiration analysis and foodintake in four captive killer whales 7620. Swimming velocities and breathing rates in free-ranging killer whales during the summerand spring 10521. Regression equations and statistics for the relationship between respiration rates andswimming velocities in male, female, and juvenile killer whales 10622. Body measurements of stranded killer whales 1118viiiLIST OF FIGURESFigure Page1. Apparatus used to collect expired air from captive killer whales, Orcinus orca 102. Oxygen consumption and carbon dioxide production as a function of apnea forHyak in different activity states 253. Oxygen consumption and carbon dioxide production as a function of apnea forFinna in different activity states 264. Oxygen consumption and carbon dioxide production as a function of apnea forYaka in different activity states 275. Oxygen consumption and carbon dioxide production as a function of apnea forVigga in different activity states 286. Rate of oxygen consumption as a function of apnea for Hyak for Activity states 1 and 3 337. Rate of oxygen consumption as a function of apnea for Finna for Activity states 1 and 3 338. Rate of oxygen consumption as a function of apnea for Yaka for Activity states I and 3 349. Rate of oxygen consumption as a function of apnea for Vigga for Activity states 1 and 3 3410. Metabolic rate as a function ofbody mass of mammals 3711. Relationship between body length and age of six killer whales 5912. Daily food consumption by male killer whales 6513. Daily food consumption by female killer whales 6614. Food intake for Yaka as a function ofwater temperature 7015. Food intake for Vigga as a function ofwater temperature 7016. Food intake for Finna as a function of water temperature, 1993 7117. Food intake for Bjossa as a function of water temperature, 1993 719ix18. Food intake for Bjossa during pregnancy and lactation, 1988 7319. Food intake for Bjossa during pregnancy and lactation, 1991 7320. Food intake as a function of estimated body mass in six killer whales 7421. Food intake as a fraction of estimated body mass in six killer whales 7422. Theodolite tracking of killer whales 8923. Potential dive profiles 9424. Relation ofbias in breathing rate to sample size for female killer whales 10325. Respiration rates as a function of swimming velocity in killer whales 10426. Metabolic rate as a function of swimming velocity in killer whales 10827. COT of male and female killer whales as a function of swimming velocity 11028. Comparison of COT based on respiration as a function of swimming velocity andfitted drag models for killer whales 11310xACKNOW LED GEMENTSMany people have been part of and contributed to this research. Mike Bigg, DavidShackleton and David Bain have been the inspiration to begin and finish this work. Theircooperative spirits put this work much further of where it would have been without them.My colleagues in the field, David Bain, Tiana Colovos, Ralph Brandt, Lisa Berry, VanessaGeary, A. Rus Hoelzel, Pam Stacey, Robin Baird, Linda Nichol, Patrick Kirby, and PaulaTrost have spent months with me working in beautiful locations but not always under easyconditions. M.D. Lamont and Dale Pratt provided access to locations for the theodolite study.Colleen Howe and Bruce Gregory were always there to provide logistical support. The WhaleMuseum in Friday Harbor, WA, provided logistical help and Rich Osborne in particularhelped with many aspects of the research on San Juan Island.Without the trainers and researchers at the aquaria this research would not have happened.Jeremy Fitz-Gibbon, Doug Pemberton, Vic Biscaro and Klaus Michaelis of the VancouverPublic Aquarium in Vancouver, B.C., and Sonny Allen, Paul Povey, Jon Lawrence, DebbieMarin-Cooney, Amy Traxler and Terry Samansky of the Marine World Foundation in Vallejo,CA, were invaluable during all the months of collecting respirations from the whales and insearching for food data records as well as providing entertainment at all times. David Bainand Patty Gallagher Cates helped with all aspects of data collection at Marine WorldAfrica/USA. Dave Bisso at the Sutter Solano Hospital in Vallejo, CA, permitted me theunlimited use of their blood-gas analyzer.xiMy committee at the University of British Columbia and Simon Fraser University waspartly put together at the last minute. Many thanks go to Bill Milsom and Alton Harestad fortheir encouragement and help with the last draft.Peter Olesiuk from the Pacific Biological Station in Nanaimo, B.C., Heinrich Binder of theUniversity of Zuerich in Switzerland, Anne York from the National Marine Mammal Lab,Don Hood from the University of Alaska and David Bain were always available fordiscussions, statistical and mathematical help.Many thanks to Horst Kriete for financial support during part of this research. The WorldWildlife Fund Canada and the Anne Vallee Memorial Fund provided financial assistance forparts of this research. Equipment was donated by Micrologic and Humminbird.xiiThis dissertation is dedicated to the memories ofUte-Marie Dauelsberg KrieteandMichael Andrew BiggxiiiPREFACEIt has been a long-standing belief that marine mammals have metabolic rates that aresignificantly higher than those of terrestrial mammals of comparable size in order tomaintain thermal homeostasis in cold aquatic conditions (Andersen 1965, Ridgway 1972,Brodie 1975, Schmidt-Nielsen 1984). The belief that marine mammals have elevatedmetabolic rates has existed for decades and even more so since Slijper (1979) publishedaccounts of all the remnants of prey found in a killer whale’s stomach. The increased heatloss in water compared to air was the main basis for suggesting higher metabolic rates inmarine mammals. More recent studies (Lavigne et a!. 1982, Yasui and Gaskin 1986,Innes et a?. 1987) suggest, however, that marine mammals have metabolic rates similar tothose of terrestrial mammals.However, it is still difficult, or impossible to measure metabolic rates in most cetaceans.Logistic problems prevent direct measurements in the wild, so other methods have be usedto estimate metabolic rates. Species held in aquaria can be used for measurements, butphysiological measurements may differ somewhat from those of the species in the wild.To shed some light on whether cetaceans, and in particular killer whales, Orcinus orca,have higher metabolic rates than do terrestrial mammals of similar sizes, this studyaffempts to determine how much food different age and sex classes of killer whalesrequire. Three studies, two of them on killer whales in different aquaria, and one on freeranging whales, were conducted independently of each other to test whether estimates ofmetabolic rates determined in each one of the methods was comparable with the results ofxivthe other methodologies. If the estimates obtained by the different techniques are similarthe methods can be conducted individually to estimate metabolic rates in killer whales.The importance of this result is not only of academic interest because as humanscontinue to exploit and deplete the natural resources of the sea, conflicts between marinemammals and fisheries have become more frequent. For example, harbour seals (Phocavitulina) are considered a problem because they remove fish from fishing gear and arebelieved to prey on valuable fish species (Beach et a!. 1985, Olesiuk et a!. 1990b) whileCalifornia sea lions’ (Zalophus calfornianus) depredation on a depleted winter-run of wildsteelhead (Oncorhynchus mykiss) has lead to temporary removal and relocation of the sealions (Norberg and Bain 1994). Recently, the question of how much killer whales eat hasbecome an important issue due to fishery conflicts with killer whales. Competitionbetween salmon fisheries and killer whales has been an issue for several decades in BritishColumbia and Washington waters (Bigg and Wolman 1975, Bigg 1982). In Alaska, killerwhale depredation on blackcod (Anoplopoina fmnzbria) in the longline fisheries hasseriously financially harmed the fishery (Matkin 1988).The first chapter reports the development of a technique to measure metabolic rates forkiller whales in different activity states. Both standard (a low estimate of metabolic rateto sustain life) and realized (the energy necessary for standard metabolism plus dailyactivities) metabolic rates are estimated for different age and sex classes of killer whalesusing this technique.In the second chapter, food data for the individual killer whales for which metabolicrates via respiration analysis were determined, as well as two other individuals, arexvanalyzed from the time they were available and trends of food consumption as a functionof body mass are determined. Other factors such as season, water temperature andreproductive status are also examined to possibly affect food intake. Food consumptionreported in this chapter and energy expenditure determined through respiration analysis inthe previous chapter are compared and net assimilation efficiencies (NAE) are inferred. Ifthe net assimilation values determined are similar to those reported in the literature forother marine mammals, then the NAE inferred and methodology used here can beassumed to be reasonable for killer whales.In the third chapter, metabolic rates are estimated for free-living killer whales byanalyzing the respiration rates of different age and sex classes as a function of swimmingvelocity. The cost of locomotion and most efficient swimming speed of male and femalekiller whales are determined. Data on respiration from captive whales are then combinedwith the respiration rates observed in the wild killer whales to convert respiration rates tometabolic rates. Realized metabolic rates are estimated using respiration rates and oxygenconsumption from different activity states of captive animals and combining those datawith daily activity budgets observed in wild killer whales.Several others (Blake 1983, Lang 1965, 1966) mathematically estimated the dragdifferent marine mammals encounter while swimming at different velocities. One of theleading thoughts has been that it is unknown how marine mammals can overcome drag,which, according to theoretical calculations, should be almost entirely turbulent.According to Gray (1936), the power that would be required to overcome drag was greaterthan the maximum power available to cetaceans from their locomotor muscles. Here, anxviattempt is made to estimate what percentages of drag are laminar and turbulent for killerwhales swimming at different velocities. Several unknown parameters need to be assumedto fit laminar and turbulent curves to those determined for the cost of locomotion in killerwhales. If drag is lower than expected, the animal would have to expend less energy forits daily moving activity, which in turn would decrease its realized metabolic rate.By approaching the estimation of metabolic rates of killer whales from differentperspectives, estimates can be compared to each other to test whether results arehomogeneous. While some uncertainties and unknowns, such as exact body weight andgrowth rates, exist, assumptions and methodologies can be considered reasonable if similarresults are obtained from the different studies.xviiChapter 1: METABOLIC RATES IN CAPTWE KILLER WHALES,Orcinus orcaINTRODUCTION AND OBJECTIVESOver the last 60 years, many studies have been conducted to measure the metabolicrates of animals. To compare metabolic rates among species, a baseline, the basalmetabolic rate, has been established by studying animals of different sizes and creating aregression equation showing the relationship between heat production and body weightunder standardized conditions (Brody 1945, Kleiber 1987). To meet standardizedconditions during testing, animals must be physically and sexually mature, in a non-reproductive and post-absorptive state, in a calm psychological condition and resting in athermal neutral chamber at temperatures at which no additional metabolic energy isnecessary to keep the body at a constant temperature and metabolic rates are independentof environmental temperature (Brody 1945, Kleiber 1987, Worthy 1990).Kleiber’s (1987) best fit regression for basal metabolic rates in terrestrial mammals isdescribed as:[1] log10 BMR = 1.83 + 0.756 log10 M ± 0.05,where BIVIR = basal metabolic rate in kcal/d, and M = body mass in kg.1This formula was approximated and simplified by Kleiber (1987) to:[2] BMR = 70 M 0.75,where BMR = basal metabolic rate in kcalld, and M = body mass in kg.To determine whether the animals are in a post-absorptive state, the respiratoryquotient (RQ, the ratio of volume at STP of carbon dioxide produced to the volume ofoxygen consumed) is measured. By simultaneously measuring both oxygen consumptionand carbon dioxide production by the animal, the resulting RQ indicates the nutrient thathas been metabolized (Schmidt-Nielsen 1990). Usually the RQ lies between 0.7 and 1.0.An RQ near 1.0 suggests primarily carbohydrate was metabolized while an RQ of 0.7suggests that fat was the primary substrate. An intermediate RQ indicates that proteins ormixtures of two or three different classes of nutrients were being metabolized (Schmidt-Nielsen 1990). An RQ indicating the burning of fat shows the animals were in apostabsorptive state when measurements for basal metabolic rates were collected. Inmammals, the time when the post-absorptive state is reached, changes depending on thetype of feed and species, but is about 12 hours in rats (Kleiber 1987, Schmidt-Nielsen1990).When animals are in a thermal neutral chamber, metabolic rates are independent ofenvironmental temperatures (Worthy 1991). Williams et a!. (1991) estimated thermalneutral zones for bottlenose dolphins (Tursiops truncatus) and determined that the animal&core temperature did not change with water temperatures ranging from 3.6° C to 17.3° C,2while the animals’ metabolic rates did not change with water temperatures rangingbetween 6°C and 17.3 °C.Because traditional methods for determining metabolic rates, such as placing animalsinto thermal neutral chambers, are impractical for large aquatic mammals, alternativeapproaches have been used in marine mammals. Metabolic rates of cetaceans, and inparticular large mysticetes, have been estimated from lung volumes measured fromharpooned or dead animals, with respiration rates determined from wild living individuals(Laurie 1933, Scholander 1940, Thompson 1961, Kanwisher and Sundnes 1965, 1966,Rice and Wolman 1971). The potential lung volume and oxygen consumption of theharpooned whales (litres of oxygen) was then converted to energy expenditure byassuming an energy equivalent for oxygen consumption (4.8 kcal/litre oxygen per breath,Brody 1945). Parry (1949) used seasonal variations in blubber thickness measured bywhalers as an indicator of energy consumption, though his conclusions are questioned byKanwisher and Sundnes (1966) for assuming a constant mammalian metabolic rate.Brodie (1975) used the net gain in oil during feeding, estimating the daily lipid ration, itscatabolic value and approximated standard metabolic rates for rorquals in subtropicalwaters.Well designed studies using double-labelled water have been conducted with pinnipeds(Costa 1987), but have been too expensive to apply to larger cetaceans. Therefore,metabolic rates have been determined in captive delphinids using indirect calorimetry,measuring the amount of oxygen used by the individual and converting this intoequivalent energy utilized by the animal.3Lenfant et al. (1968) measured tidal volumes, the volume of air inhaled in a singlebreath, of a subadult female killer whale (Orcinus orca) while beaching her during theprocess of gas collection. Being beached may have decreased the animals’ ability toexhale and inhale fully by as much as 20% due to the pressure of her weight out of thewater (Wahrenbrock et a!. 1974). Because training techniques and conditions for captivecetaceans have improved over the last 30 years, animals now can be trained so thatrespiratory gases can be collected with the whale at the water surface rather than beachedat the bottom of the pool. Young animals do not have to be used because individualshave survived well into adulthood and are accessible for data collection. Kasting et a!.(1989) collected respirations from one adult male and two subadult trained killer whalesand analyzed the respirations for energy requirements. He also suggested highermetabolic rates for killer whales than for terrestrial mammals of similar sizes. However,he did not correct for the decreased respiration rates during absolute rest (see methods thischapter) and used estimated weights that were probably too low for the animals inquestion (see methods this chapter). Other metabolic studies on wild cetaceans have beeninconclusive and researchers often assumed respiratory variables from other species, henceestimating metabolic rates indirectly from physiological data (e.g. Lockyer 1981a, 1981b,Yasui and Gaskin 1986).Brodie (1975) suggested using the term “standard metabolism” or “maintenancemetabolism” for cetaceans rather than basal metabolism. He argued that many cetaceansare negatively buoyant and must move in order to reach the surface to breathe. Brodie(1975) states that basal metabolic rate is therefore probably never attained by cetaceans,4and the cost of the minimal exertion required to move to the water’s surface to breathe isinseparable from the animal’s basal metabolism. However, killer whales are neutrallybuoyant in the still water of an aquarium depending on how inflated their lungs are (D.Bain pers. comm.), so standard metabolic rates (SMR), which should be quite similar toBMR’s, can be attained. Lockyer (1981a, 1981b) had similar concerns to Brodie’s (1975).She stated that instead of measuring BMR, the resting metabolic rate (RMR) is moreappropriate for whales and dolphins, because BMRs are measured under minimalmetabolic energy expenditure which is rarely encountered in cetaceans. Lockyer furthersuggests that using the RIV[R, which according to Brody (1945) is the true BMR in adultterrestrial animals plus 15% for the expense in muscular effort necessary to move about tobreathe, is an appropriate measure for metabolic rates in cetaceans. Peters (1989) alsosuggests using SMR to replace BMR in situations where the measurements are notnecessarily minimal but when they are collected under standardized conditions to yieldlow values. The term “standard metabolic rate” (SMR) will be used for the animalsreported in this paper.In many of the early energetics studies marine mammals were determined to havehigher metabolic rates than do terrestrial mammals of similar size (Kanwisher andSundnes 1965, 1966, Sergeant 1969, Irving 1973, Kasting et al. 1989). These highermetabolic rates, with low metabolic scopes (the ratio of metabolic rates between maximalexertion and rest) were interpreted as being due to water drawing heat away from thebody 25 times faster than does air, and to the animals needing to increase theirmetabolism to maintain a constant internal body temperature (Ridgway 1972). An5unfavourable (large) surface to volume ratio for smaller cetaceans was also suggested toelevate metabolic rates. More recently, other researchers (Olsen et al. 1969, Hampton andWhittow 1976, Lavigne et a!. 1986; Innes et a!. 1987, Worthy ci a!. 1987) rejected theidea that cetaceans have elevated metabolic rates. All pointed out that high rates in manyof the past cetacean studies were calculated under environmental conditions different thanthose specified by Kleiber (1987), or that juvenile animals were used. They providedempirical data to show that metabolic rates of some marine mammals are comparable tothose of terrestrial species, an indication that marine mammals are well adapted physicallyand physiologically to their marine environment. Some of these adaptations include asmall surface to volume ratio and a thick blubber layer with a high lipid content foreffective insulation, all of which allow cetaceans to have a thermal neutral zone undermost normal ranges of water temperatures (Worthy 1990).The opposing conclusions for marine mammal metabolic rates and scopes can besummarized relative to terrestrial mammals (Brody 1945, Kleiber 1987) as:a) high basal metabolic rates and low metabolic scopes, versusb) normal basal metabolic rates and normal metabolic scopes.This study is intended to discriminate between these 2 hypotheses in the case of killerwhales. Also, additional baseline data were collected to examine fundamental aspects ofcetacean bioenergetics. Specifically, I collected data based on respiration analysis to:61) determine respiration rates during rest, at moderate, and at high activity states,2) determine daily activity budgets,3) estimate standard metabolic rates and metabolic scopes, and4) estimate daily caloric expenditures.METHODSStudy AnimalsFour different study animals were used for respiration collection and activity budgetdetermination.: one adult male (Hyak, 20 years old at time of the study) and one subadultmale (Finna, 11 years old at time of study) from the Vancouver Aquarium, Vancouver,B.C., as well as one adult female (Yaka, 21 years old at time of study) and one subadultfemale (Vigga ,11 years old at time of study) from Marine World Africa/USA in Vallejo,California.Metabolic Rate DeterminationMetabolic rates of killer whales were estimated by collecting respiratory gases aftervarious apneas during different activity states. Tidal volumes, oxygen uptake and carbondioxide production rates were determined, and standard metabolic rates and daily caloricexpenditures were estimated. Respiratory quotients and the metabolic scope for eachanimal were determined. Standard metabolic rates were compared to Kleibe?s (1987)equation on basal metabolic rates in mammals.7Several variables, described below, were collected and measured to determine metabolicrates. Metabolic rates were calculated by the generalized equation:[3] MR = 5 * Vol 02 * C,where: MR metabolic rate (kcalld), = mean number of breaths per day, and Vol 02 =mean litres of oxygen consumed per breath, c = conversion factor for litres of 02 to kcal(1 litre of 02= 4.8 kcal, Brody 1945, Pike and Brown 1975).a) Respiration Rate DeterminationRespirations were counted and timed for a minimum of 15 mm prior to samplingrespirations for gas analysis to determine respiration rates at rest (Activity state 1) (activitystates are defined below). Respirations at medium and high activity states (Activity states2 and 3, respectively) were counted while the animals were involved in the activity state(i.e. approximately 15 mm during a training session or during the show). Respirationrates were counted during two other activity states, nightly rest and extremely activebehaviours (Activities states 0 and 4, respectively). These respiration rates were used onlyto determine metabolic scopes, therefore only the minimum and maximum respiration ratesobserved were used for metabolic estimates of standard and extremely active metabolicrates.To compare observed frequencies of respirations during rest to those of terrestrialmammals, predicted respiration rates for the four killer whales were calculated fromStahl’s (1967) allometric equation for mammals:8[4] Frequency of Respiration (breaths/mm) = 53.5 M°6,where M = body mass in kg.b) Daily Activity Budget DeterminationThe amount of time that the four killer whales spent in the different activity states wasrecorded throughout the days when breaths were collected, as well as during the earlyevenings at the Vancouver Aquarium and throughout the nights at Marine World.Activity budgets were estimated based on the number of hours Hyak and Finna spent inActivity states 1 and 3, while Yaka’s and Vigga’s daily activity budgets were separatedinto Activity states 1, 2, and 3.c) Collection of Expired AirDuring the fall of 1987, respiratory gases were collected from Hyak and Finna at theVancouver Aquarium. From November 1988 to March 1989 and from September 1989 toNovember 1989, collections of respiratory gases were made from Yaka and Vigga atMarine World/Africa USA. To collect respiratory gases, an apparatus was built using 10cm diameter PVC piping with two one-way valves for inhalation and exhalation (Figure1). The bottom edge of the funnel was lined with soft foam to act as a seal when theapparatus was placed over the whale’s blowhole to avoid the loss of exhaled air.Meteorological balloons, with a maximum capacity of 150 1, were attached to theexhalation tube(s) to collect the exhaled air. Two balloons were necessary for Hyak andYaka because of the size of their tidal volumes. One-way valves were used in case the9ADFigure 1. Apparatus used to collect expired air from captive killer whales, Orcinusorca. Body of apparatus is made from 10 cm diameter PVC pipe and aplastic funnel. A - Collection vessel (metereological balloon - 2 used for adultwhales); B - Valve for collecting air samples for gas analysis; C - One-wayvalves; D - Handles to hold apparatus on whale’s blowhole; E - soft foamseal around base of plastic funnel.E10animal wanted to inhale immediately following the collection of respiratory gases andbefore removal of the funnel, or if it became frightened when the funnel was placed overits blowhole and it attempted to inhale. In this way, the animal could not inhale the airalready collected in the balloon(s). A similar method of collecting respiratory gases wasused by Spencer (1967) and by Kasting et al. (1989) for killer whales, and by Sumich(1983, 1986) for gray whale (Eschrichtius robustus) calves.The whales were trained to accept the apparatus over their blowhole and to await asignal before exhalation. This procedure was intended to allow the researcher and trainerto control the duration of apnea. Samples were not used if an audibly noticeable amountof air escaped around the edges of the funnel or if the animal exhaled again after removalof the funnel and before inhaling.Exhaled air was collected for tidal volume and respiratory gas analysis after threeactivity states operationally defined as:Activity state 1: Resting for a 15 mm period and at least 14 h after the last meal to meetconditions of post-absorptive state for standard metabolic ratedetermination.Activity state 2: Light to moderate activity, involving a light training session, orswimming leisurely around the pooi for at least 15 mm prior togas collection. Gas collections for Activity state 2 were alwaysmade after the animals had been fed at least once within the last 3h.11Activity state 3: Immediately after the last activity of a show with high levels of activity,i.e. involving many breaches. Gas collections for Activity state 3were always made after the animals had been fed at least oncewithin the last 3 h.For logistical reasons at the Vancouver Aquarium, collections of exhaled air were onlypossible after Activity states 1 and 3.Two additional activity states were also defined, although no respiratory gases werecollected due to the absence of training personnel. During these additional activity states,respirations of the individual whales were counted by an observer situated on a hiddenplatform after the training personnel had left for the day, i.e., in the evening and at night.The animals’ behaviour during these periods ranged from 1 to 2 h of rest to more activebehaviour (breaches) than that seen during shows. The two additional activity states wereoperationally defined as:Activity state 0: Resting behaviour where the animals were stationary at the water surfacefor at least 15 mm and appeared to be in the calm psychologicalstate as described by Kleiber (1987). This was less than 14 h afterthe last feed.Activity state 4: This activity state consisted of extremely active, “percussive” behaviours,consisting of breaches, tail and flipper slaps, and fast swimming.Activity state 4 sometimes occurred longer (>15 mm) than similarbehaviours during shows.12The difference between comparable behaviours seen during the day and night was thatduring night time no behaviour was requested of the whales and therefore the behaviourwas spontaneous.d) Tidal Volumes, Oxygen and Carbon Dioxide RatiosAfter the whales exhaled through the funnel into the balloons, the collected gases wereforced through a dry gas meter (calibrated with a Century 100H gas flowmeter) todetermine the tidal volume. Tidal volumes were measured for each breath at eachdifferent activity state to determine if tidal volumes changed with activity state.While the exhaled air was forced through the dry gas meter, four 60 ml gas samples ofthe exhaled air were drawn off with a syringe via a valve directly from the funnel. Thesesamples were collected at equal intervals, i.e., after approximately 20%, 40%, 60% and80% of the air in the balloon(s) had been forced through the dry gas meter, to get amixed sample of exhaled air. These samples were analyzed for the difference of oxygenand carbon dioxide from atmospheric air after being corrected to standard temperature andpressure (dry). The mean value of oxygen and carbon dioxide present in the foursamples was determined. In Vancouver, samples were analyzed both with a BeckmanCarbon Dioxide Analyzer (LB-2) and a Beckman Oxygen Analyzer (OM-il). At MarineWorld, the samples were analyzed with an Instrumentation Laboratory System 1302p11/blood gas analyzer provided by the Suffer Solano Hospital. All instruments used werecalibrated before samples were run to minimize sources of variation and error.Mean values of oxygen extraction, the oxygen available in the inhaled air, were13calculated for the three different activity states to relate the difference in oxygen extractionto differences in activity. Mean oxygen extraction at mean apnea during the differentactivity states was calculated as:[5] E =(1—) xlOOp1Q2where: E01 is the extraction of oxygen in %, PE°2 is the partial pressure (mm Hg) of theexhaled oxygen, and p1O2 is the partial pressure (mm Hg) of the inspired oxygen.Carbon dioxide production by the whales was calculated as:[61 Co2 Production = (PE.- PATh x 100 / Atmospheric Pressurewhere: CO2 is the % of exhaled air produced by the animal, Po is the exhaled partialpressure (mm Hg) of carbon dioxide, PAmco is the partial pressure (mm Hg) of CO2 inatmospheric air, and atmospheric pressure is in mm Hg..Oxygen extraction and carbon dioxide production as a function of apnea were plotted forall animals in each activity state. A log-log transformed regression line, providing thebest fit to the data, was fitted to the data. The amount of oxygen consumed , the amountof 02 (1) taken into the body divided by apnea was calculated as a function of apnea andgraphed.Metabolic rates were calculated using:14[7] Mean Metabolic Rate = (Tidal Volume x [F1-2]) / apneawhere: Metabolic Rate is in litres of 02/s, tidal volume is in litres, Ft0 is the fraction ofinspired oxygen, F0 is the fraction of oxygen in expired air, and apnea is measured in s.To compare the killer whales’ observed tidal volumes at rest and the animals’ vitalcapacity, the maximum volume that can be inhaled in one breath (Peters 1989) which wasoperationally defined as the largest inhalation measured, to those of terrestrial mammals ofsimilar sizes, predicted values for killer whales were calculated from Stahl’s (1967)allometric equations:[8] Tidal Volume at rest (ml) = 7.69 M’°4,where M = body mass in kg.[9] Vital Capacity (ml) = 56.7 M’°3,where M = body mass in kg.Ventilation rates were calculated for the killer whales from respiration rates and tidalvolume and compared to Stahl’s (1967) allometric equation for terrestrial mammals:[10] Ventilation Rate (mi/mm) = 379 M°80,where M body mass in kg.15e) Weight EstimatesTo estimate caloric expenditures on a per kilogram basis, body mass was calculatedusing Bigg and Wolman’s (1975) formula. This formula was derived from empirical dataand was based on the actual weights of 32 live-captured and stranded killer whales:[11] M = 0.000208 L2577,where: M is body mass in kg and L is total body length in cm.Total body lengths for the captive animals were obtained by measuring from the tip of therostrum to the notch of the flukes (Norris 1961). For the captive animals, 20% was addedto the mass calculated by Bigg’s and Wolman’s (1975) formula. Data on actual weightmeasurements for animals in captivity (Heyning and Dahiheim, in press, J. Antrim, SeaWorld, pers. comm. and J. Fitz-Gibbon, Vancouver Aquarium, pers. comm.) showed thatthe whales were on average 20% (17%, 19% and 25%) above the weights calculatedbased on the whales’ length (Bigg and Wolman 1975). Growth rates have also beenreported to be faster in captivity and age of maturity is reached earlier than in animals inthe wild (Asper et al. 1988, see also Chapter 2). The adjusted masses lie approximatelyone standard deviation (21.58% of the mean) above Bigg’s and Wolman’s (1975) studyanimals’ masses.f) Standard Metabolic Rate EstimatesEstimates for standard metabolic rates were made both with mean and maximum tidal16volumes. Minimum respiration rates collected during Activity state 0 were combined withoxygen consumption rates measured during Activity state 1. For further analysis, theoxygen data were applied to equation [3] to estimate SMR. The SMR was divided by theestimated mass of the whales to yield the animal’s mass specific metabolic rate(kcal/kg/day).To determine whether the data fit with those of terrestrial mammals, SMRs calculatedfor Hyak and Yaka, the two adult whales, were plotted on Kleiber’s (1987) regression lineof the relationship between the logarithms of metabolic rate and body mass of terrestrialmammals.g) Daily Energetic ExpenditureActivity budget studies were conducted at Marine World over a period of 3 months todetermine how much time the animals spent in different activity states. Measurementswere taken in bouts of 15 mm every hour over a period of 12 h two times a week (afterBain 1986), to relate respirations to activities. At the Vancouver Aquarium, nightlyobservations were not allowed, so observations were conducted from 06:30 until 20:30 fortwo days during the respiration collection study in October 1987. The number of hoursspent in the different activity states for which respirations rates were collected wasdetermined. Maximum tidal volumes were used for all calculations of metabolic rates.Mean respiration rates collected during Activity states 1, 2, and 3 were multiplied by theoxygen consumption per breath at the mean apnea measured during the respective activitystate. The oxygen data were applied to equation [3] to estimate metabolic rates for17Activity states 1, 2, and 3. Daily metabolic rate can be estimated as:[12] Daily IVIR = (TimeACVIY * IV.[R Activity i) + (TimeActiviw 2 *IRACtIVI 2) + (TimeACVY 3 * IVLRAt ty 3)’where: Daily Metabolic Rate is in kcalid, Time is in hid, and the Metabolic Rate for thedifferent activities is in kcalih.The metabolic rate calculation is given in equation [3]. Metabolic rates for the differentactivity states were also calculated on an hourly basis.Metabolic ScopeThe increase in metabolic rate between rest and maximal exertion was determined forthe four whales used for this study by extrapolating how many times higher the maximalrate of oxygen consumption is compared to the standard metabolic rate (Schmidt-Nielsen1984). Tn addition, metabolic scopes for the four study animals were determined for theactivity states (1 and 3) for which gas analysis was possible.Respiratory OuotientRespiratory quotients were determined for each exhalation measured for each individual.This ratio [mols of CO2 produced divided by the mols of 02 consumed (Kleiber 1987)]indicates whether fat, protein or carbohydrates were burnt. Respiratory quotients wereaveraged by activity states for all individual whales combined.18RESULTSRespiration RatesRespiration rates and ranges differed for each killer whale in each activity state(Table 1). Respiration rates between Activity states 1 and 0 decreased by 61% for Hyak,by 51% for Yaka and Finna, and by 40% for Vigga. Spencer et al. (1967) observedrespiration rates of an undisturbed, confined adult male (total length = 656 cm, weightestimate = 3414 kg) and determined that the animal’s average respiration rate at rest was1.06 breaths/mm. This is similar to Hyak’s respiration rate during Activity state 1 (1.02breaths/mm).Respiration rates during Activity state 4 were between 16% and 40% higher thanduring Activity state 3 (Table 1). The whales’ frequencies of respiration during rest(Activity state 0) were between 11.8 to 14.8 times lower than that predicted fromallometric equations.Rest periods were longer and continuous during the night, lasting up to 2 h, while restperiods during the day were shorter and intermittent, lasting only up to 30 mm.Apnea and Tidal VolumeApnea could be controlled by the trainer and researcher only after Activity state 1 andfor the short apneas (<30 s) after Activity states 2 and 3. The whales determinedmaximum apnea duration for Activity states 2 and 3 because they did not seem willing to19Table1.Summaryofrespiratorydatafromfourcaptivekillerwhales.AnimalActivitynApneaMeanRangeStandardMeanRangeStandardRangeTidalVolumeDeviationRespirationRespirationDeviation(s)(I)(I)(I)RateRate(breaths/h)(breaths/h)Hyak0---24-113515-149211.5153.5-254.521.06142.8-87.89.831524-50205.582.0-258.542.18462.1-90.04.24--1003.6Finna0---30-0.613510-12094.540.0-133.022.76135.0-82.012.63228-4061.926.0-91.519.69081.8-100.07.804---109-3.5Yaka0-----30--12110-11997.554.0-149.026.66143.9-97.314.121310-9078.050.5-114.019.510072.0-102.92.831214-46102.675.5-135.017.312997.3-156.55.34---180Vigga0-36--11028-11532.816.0-42.07.46045.0-100.06.42928-4441.330.0-55.08.57260.0-90.03.331515-3942.517.5-60.012.2138109.1-156.04.24--160hold their breaths for extended periods after exercise (Table 1). For collections ofexhalations during Activity state 1, the durations of apnea ranged from 10 to 149 s, whilethe range of apnea after Activity state 2 was limited from 10 s to 48 s and from 8 s to46 s after Activity state 3.Tidal volumes were tested for variation with individual and activity state using a 2-wayANOVA (Table 2). A significant individual effect and interaction term were found; itappeared that whether there was any difference between tidal volume and activity statedepends on the individual. Tukey’s test for multiple comparisons (Zar 1984), using 187cases and 10 groups of observations, showed that only Finna’s tidal volumes weresignificantly different between the two activity states (Table 3). Tukey’s multiplecomparisons test (Zar 1984) was used to determine if differences exist in tidal volumesbetween individuals, when engaged in the same activity. All tidal volume comparisonswere significantly different from each other except for Finna’s and Yaka’s volumes inActivity state 1, and Finna’s and Vigga’s tidal volumes in Activity state 3 (Table 4).Tidal volumes at rest were determined for the animals from this study using Stahl’s(1967) allometric equation. The mean tidal volumes measured for the four whales werebetween 1.3 and 4.2 times those of predicted values, while the whales’ maximum tidalvolumes measured were between 1.3 and 5 times the predicted tidal volume at rest. Inboth cases Vigga’s differences in tidal volume from predicted values were at most half thatfor the other three whales (Hyak, Finna and Yaka). Comparing the whales’ vital capacityto predicted values (Stahl 1967) and assuming tidal volume is 80% of the vital capacity ashas been determined for other cetacean species (Irving et al. 1941, Olsen et al. 1969,21Table 2. Two-way ANOVA to test for variation of tidal volume among individual whales betweenActivity states 1 and 3.Source Sum of Squares DF Mean Squares F-Ratio SignificanceLevelwhales 589846.043 3 196615.348 355.488 p<O.000lactivitystates 1212.842 1 1212.842 2.193 p=O.l4lwhales *activity states 11121.132 3 3707.44 6.702 p<O.000lError 86834.561 157 553.086Table 3. Differences in tidal volume (1) for individual whales in different activity states (see Table 1for sample size, SD and ranges) from Tukey’s test for multiple comparisons.NS = not significantAnimal Comparison between SignificanceMean Tidal Volumes LevelHyak Activity State 1 Activity State 3211.46 205.50 NSFinna Activity State 1 Activity State 394.48 61.86 p<0.O03Yalca Activity State 1 Activity State 297.54 78.04 NSActivity State 1 Activity State 397.54 102.63 NSActivity State 2 Activity State 378.04 102.63 NSVigga Activity State 1 Activity State 232.80 41.20 NSActivity State 1 Activity State 332.80 42.50 NSActivity State 2 Activity State 341.20 42.50 NS22Table 4. Significance of differences in tidal volumes betveen individualwhales in the same activity state. NS = not significantAnimals ActivityState Significance levelHyakandYaka 1 p<O.OO13 p<O.OOlHyak and Finna 1 p<O.OO13 p<O.OOlHyak and Vigga 1 p < 0.00 13 p<O.OOlFinna and Yaka 1 NS3 p<O.OO1Finna and Vigga 1 p <0.0013 NSYaka and Vigga 1 p<0.OOl2 p<O.O13 p<O.OOl23Ridgway et a?. 1969), Hyak’s, Finna’s and Yaka’s vital capacities are between 68% and94% of the values predicted from the allometric equation (Stahl 1967), while Vigg&s vitalcapacity was only 35% of the predicted value from Stahl’s allometric equation for vitalcapacity. Values for observed ventilation rates are between 0.26 and 0.32 those ofpredicted values.Respiratory GasesThe extraction of oxygen and production of carbon dioxide were graphed as a functionof apnea for the four individual whales (Figures 2-5, Table 5). Both oxygen extractionand carbon dioxide production were related to the duration of time between breaths(apnea). The different significant regression lines for oxygen extraction were compared toeach other. Within individuals, slopes between activity rates were compared (Table 6).All slopes were significantly different, except those for Finna (Activity states 1 and 3).However, the intercepts were statistically different. Between individual whales, matchingbehaviour states were compared by using Tukey’s test for multiple comparisons (Zar1984). For Activity state 1, Yaka, Finna and Hyak were all significantly different fromeach other. For Yaka, Activity state 3 was significantly different from the other twoactivity states. For Hyak, Activity states 1 and 3 were also significantly different. Allother comparisons tested were not significantly different from each other.Comparisons among mean oxygen consumption and carbon dioxide production at meanapnea, based on mean tidal volumes for different activity states, showed that 02consumption and CO2production for Finna were lower at Activity state 3 than during24IIYAK-CO2PRODUCTIONHYAK-OXYGENEXTRACTIONActivityState114ActivityState170C11.26O0..40•—•—:8.4•_30—‘“—5.6—-.I.”•U202.8r20.09010p<O.Ol40_________________0020406080100120140160Apnea(s)020406080100120140160Apnea(s)IIYAK-CO2PRODUCTIONHYAK-OXYGENEXTRACTIONActivityState3ActivityState 31470—60N -11.20_Ih•408.4.ç30rO.215.6—r’0.1820P<O•l20102.800204060801001201401600Apnea(s)020406080100120140160Apnea(s)Figure2.Oxygenextractionandcarbondioxideproductionasafunctionofapneafor Hyakindifferentactivitystates.Figure3.Oxygenextractionandcarbondioxideproductionasafunctionof apneaforFinnain%_J..••—----•—-r’=0.58p<o.0001FINNA-OXYGENEXTRACTION70ActivItyState1—60e50e r 30 20 010 0- 020406080100120140160Apnea(s)•-•--FINNA-CO2PRODUCTION14ActivityState111.2,0020406080100120140160Apnea(s)r=0.60p<o.0001FINNA-OXYGENEXTRACTIONActivityState370—60 50C40 3020010 0--•020406080100120140160Apnea(s)FINNA-CO2PRODUCTIONActivityState31411.2C8.45.62.8C-,0020406080100120140160Apnea(s)r0.52p<o.0002differentactivitystates.YAKA-OXYGENEXTRACTION170 6050—-30-.20z0.52p0.000210020406080100120140160A()YAKA-CO2PRODUCTIONA00viIy$l0I14112r—035.p<0.003804C56828026406000100120140150—.YAKA-OXYGENEXTRACTION—&.270 00too 40r07200 7020406000100120140760—YAKA-CO2PRODUCTIONA00viIyS00.214112r=0.1504pOO.OS256..I.—0 ‘-28020406060100120140160—YAKA-OXYGENEXTRACTION600.370 60,50•1° 30r0.2420 10020406080100120140100—(,)YAKA-CO2PRODUCTIONAohv000e31411-2z 64---2.‘r’-0.0756-28020406002100120140100—.(,)Figure4.Oxygenextractionandcarbondioxideproductionasafunctionof apneaforYakaindifferentactivitystates.00Figure5.Oxygenextractionandcarbondioxideproductionasafunctionofapneafor Viggaindifferentactivitystates.VIGGA-OXYGENEXTRACTIONAo6iiIy88666120 60-50140—.:•020406080100120140160Ap.,16(1)VIGGA-COPRODUCTIONAdivIly1666.1141112ro.Izp<o.378.45,0.•-.•—-68 020020406080100120140160(6)VIGGA-OXYGENEXTRACTIONAdivily8868.270 605° i° 1130—r10.14—p00.30120 to020406080600620140660.(.)VIGGA-COzPRODUCTIONAdiv.tySW.21412 04 5.6,‘—0318p<O.03002.8020406080600120140160—(.)VIGGA-OXYGENEXTRACTIONAOlilSty56668370 60150 1:Ir6_0.27120p08.0510020406080100120640160VIGGA-CO2PRODUCTION14AoIiV.lySW.31112 845,68.—0.087828p020406080100120140160..TableS.Regressionequationsandstatisticsfortherelationshipbetweenoxygenextractionandapneaandcarbondioxideproductionandapneainfourkillerwhales.AnimalHyakFinnaYakaViggaEquationraOxygenextractionlogO=3.32+0.06*logapnea0.08logO23.04+0.17*logapnea0.58logO2=2.36+0.28logapnea0.52logO,.2.80+0.20*logapnea0.3r2SignificanceLevelp<o.074p<0.0001p<O.O05p<0.37StandardErrorinterceptslope0.*logapnea0.72logO2.=2.73+0.26*logapnea0.14p<0.002p<0.32AnimalHyakFinnaYakaViggaEquationr1Oxygenextractionlog022.81+0.28*logapnea0.21log02=3.27+0.18*logapnea0.52logO=3.10+0.20*logapnea0.24logO,.3.16+0.19*logapnea0.27SignificanceLevelp<0.85p<0.002p<0.lp<0.05StandardErrorinterceptslope0.<O.ll0.140.04IlogCOz=1.57+O.06*logapnea0.09p<O.000l0.090.03IlogCOL=1.27+0.l7*logapnea0.6p<0.00020.150.06IlogCO=l.09+0.l3*logapnea0.35p<*logapnea0.1ActivityState2EquationrSignificanceStandardErrorEquationOxygenextractionLevelinterceptslopeICOproductionr’SignificanceStandardErrorLevelinterceptslope0.090.05IlogCOl.53+0.06*logapnea0.15p<*logapnea0.51p<0.0320.040.08ActivityState3StandardErrorIEquationrSignificanceinterceptslopeICOproductionLevel0.110.28IlogCOl.25+0.23*logapnea0.18p<O.120.090.18IlogCOl.51+0.l8*logapnea0.52p<O.00020.110.12IlogCO,.1.57+0.12*logapnea0.07p<0410.080.09logCOl.83+O.03logapnea0.007p<O.T7Table 6. Comparison of slopes of oxygen extraction as a functionof apnea between different activity states for two killer whales.Animal Activity q SignificanceStates LevelFinna land3 1.46 p<O.2’Yaka land2 3.37 p<O.005*The intercept tested significantly different (t = 8.22, p < 0.00 1).30Activity state 1 (Table 7). The mean value of the tidal volume probably underestimatesnormal tidal volumes. It was assumed that maximum tidal volumes better reflect normaltidal volumes than mean tidal volumes do. As a result of these assumptions, the values ofthe maximum tidal volumes of the killer whales are used for all further calculations (Table8). Mean oxygen extraction at mean apnea during different activity states for the fourkiller whales showed that oxygen extraction increased between 14.4 % and 25.3% betweenActivity states 1 and 3 (mean = 20.3%) (Table 9).The rate of oxygen consumption was graphed as a function of apnea (Figures 6-9).Changes in oxygen consumption with apnea as a function of activity state showed that:a) more oxygen is used at higher activity states than at lower activity states;b) the difference in oxygen consumption generally increases with increasing apnea; andc) the rate of increase in the differences declines with increasing apnea.Mean oxygen extraction during the mean apneas observed for the different activitystates increased with an increase in activity.Standard Metabolic RatesStandard metabolic rates, estimated both with mean and maximum tidal volumes, werecalculated from equation [3] and compared to estimates of Hemmingsen (1960), Stahl(1967), McAlister (1981), Kleiber (1987) and Kasting (1989) (Table 10), although onlyestimates based on maximum tidal volumes are discussed here (see previous assumptions).Predicted estimates of basal metabolic rates from regression equations by Kleiber (1987),Hemmingsen (1960) and Stahl (1967) were lower than those measured for three of the31Table 7. Comparison between mean apnea and mean oxygen consumption and carbon dioxide productionat mean tidal volumes for different activity states for four killer whales.Oxygen Consumption (1/breath) I Carbon Dioxide Production (1/breath)Animal Activity State 1 Activity State 2 Activity State 3 Activity State 1 Activity State 2 Activity State 3Hyak 74.5 - 96.8 I 13.0 17.0Finna 39.3 - 31.6 I 6.8 5.0Yaka 32.6 29.7 44.9 I 5.0 4.5 7.3Vigga 12.1 17.3 18.3 I 1.9 2.7 2.9Table 8. Comparison between mean apnea and mean oxygen consumption and carbon dioxide productionat maximum tidal volumes for different activity states for four killer whales.Oxygen Consumption (I/breath) I Carbon Dioxide Production (1/breath)Animal Activity State 1 Activity State 2 Activity State 3 I Activity State 1 Activity State 2 Activity State 3Hyak 91.0 - 121.8 I 15.8 21.3Finna 55.3 - 67.8 9.6 11.7Yaka 49.8 56.8 65.3 I 7.6 8.5 10.6Vigga 22.1 25.2 25.8 I 3.4 4.0 4.1Table 9. Mean oxygen extraction at mean apnea during different activitystates for four killer whales.Animal Oxygen Extraction (% 0/breath)Activity State 1 Activity State 2 Activity State 3Hyak 35.2 - 47.1Finna 41.6 - 51.0Yaka 33.4 38.1 43.8Vigga 36.8 42.0 43.0mean 36.8 40.1 46.23221.81.61.411.2i Activity 10.8 -•••—-••--•-••--••-- Activity30.6 ...0.4 B ........ ..0.2 -0 I I I I I I I I I I I10 30 50 70 90 110 130 150Apnea (s)Figure 6. Rate of oxygen consumption as a functionof apnea for Hyak for Activity states 1 and ....jl.2Activity 110.8 Activity30.6 Q0.40.20 I I I I I I I I I10 30 50 70 90 110 130 150Apnea (s)Figure 7. Rate of oxygen consumption as a functionof apnea for Finna for Activity states 1 and 3.3321.81.6‘14I-D1.2——..—.--..--.-—-.——.---.-..--—--.-.ActivitylHI IActivity20.8 ---.--0.6 ° ........[t304 ..0.2........0 i I I I I I I I10 30 50 70 90 110 130 150Apnea (s)Figure 8. Rate of oxygen consumption as a function ofapnea for Yaka for Activity states 1 through .. ..0.4 .....-0.35_____0.3 4 -.- ACty10.25 - Activity20.2 --Activity 360c0.05 --.. .::0 I I I I I I I I I I I I10 30 50 70 90 110 130 150Apnea Cs)Figure 9. Rate of oxygen consumption as a function ofapnea for Vigga for Activity states 1 through 3.34Table10.Estimates(kcalilcg/d)ofstandard(SMR)andbasal(BMR)metabolicratesforkillerwhalesSMRSMRBMRBMRBMRBMRBMR(THISSTUDY)(THISSTUDY)(KASTINGetal.(McAlister)(KLEIBER)(Hemmingsen)(Stahl)(MEANTV)(MAXIMUMTV)(1989)(1981)(1987)*(1969)*(1967)*HYAK9.811.225.915.68.4510.210.5YAKA7.110.917.89.1911.111.4FINNA9.012.129.417.89.19**11.111.4VIGGA6.88.720.39•99**12.112.4TV=Tidal Volume*Estimatesderivedfromgeneralequation**MimaldidnotfitKleiber’scriteriafour killer whales in this study. Hyak’s estimated standard metabolic rate is 1.3 times thevalue predicted by Kleiber (1987) for an animal of his size, while Yak&s estimatedstandard metabolic rate is 1.2 times that predicted by Kleiber (Table 10). Though notdirectly comparable because Finna is a subadult, his standard metabolic rate is 1.3 timesKleiber’s estimate, while Vigg&s is 0.87 times Kleiber’s estimate.For the two adult killer whales, Hyak and Yaka, the standard metabolic rates wereplotted on Kleiber’s metabolic regression line (Figure 10).Activity Budgets and Estimated Daily Caloric ExpendituresCaloric expenditure varied among individuals and among activity states (Table 11).Daily caloric expenditures for individual killer whales depended on the amount of time theanimals spent in different activity states (Tables 12 and 13).Metabolic ScopesMinimum estimates for metabolic scopes were calculated for respiration rates andcaloric expenditure (Table 14). The first column is based on measured metabolic rates forActivity states 3 and 1, and the second column is based on extrapolated values forActivity states 4 and 0.Respiratory QuotientsPooled estimates on respiratory quotients for the four animals only changed slightlythroughout the day, ranging from 0.79 before feeding in the morning to 0.82 in the36IBodyMass(kg)LxTerrestrialMammals•HyakandYakaElephantUDolphinandWhale110100100010000100000Figure10.Metabolicrateasafunctionofbodymassofmammals(afterKleiber1987).Table 11. Hourly caloric expenditure of four killer whales in different activity states.kcallh kcallkg/hActivity I Activity 2 Activity 3 Activity 1 Activity 2 Activity 3Hyak 5502.6 - 10,270.9 1.17 2.19Frnna 3402.4 - 4232.8 1.00 - 1.26Yaka 3060.1 4378.0 7662.8 0.91 1.30 2.28Vigga 1483.3 1875.9 3599.4 0.62 0.78 1.50Table 12. Average number of hours spent in different activity states by four killer whales.Activity 1 Activity 2 Activity 3Hyak 22 - 2Finna 16 - 8Yaka 8 12 4Vigga 7 12 5Table 13. Daily energetic expenditure of four killer thales.kcalld kcaLfkgldHyak 141,600 30.2Finna 88,301 26.3Yaka 107,669 32.0Vigga 50,891 21.2Table 14. Metabolic scopes of four killer whales based on respiration rates and caloric expenditures.Respiration Rates Caloric ExpenditureActivity 3/1 Activity 4/0 Activity 3/1 Activity 4/0Hyak 2.1 4.2 1.4 5.0Finna 2.9 3.6 1.5 3.8Yaka 3.6 6.0 2.1 6.0Vigga 3.5 4.4 2.3 4.638afternoon after several feedings throughout the day (n=187; standard deviation rangedfrom 0.075 to 0.06). The differences in values of the respiratory quotients betweenmorning and afternoons were statistically insignificant and did not reach the value of 0.7(at which the burning of fat would be indicated) in the morning after the night-time fast.Therefore, the burning of fat alone 14 h after the last feed was not conclusively indicated.DISCUSSIONTidal Volumes and Respiration RatesStahl (1967) scaled respiratory variables in mammals and expressed them as allometricequations. The differences in tidal volumes between Stahl’s predicted and measuredvalues in this study may be primarily due to relatively uniform tidal volumes acrossactivity states in the killer whales studied. The large exchange of air per breath allows forthe longer respiratory intervals observed (Irving et a!. 1941, Olsen et a!. 1969, Ridgway etal. 1969). In turn, the long respiratory intervals lead to reduced ventilation rates byallowing extraction of a larger proportion of the oxygen in inspired air (Figures 6-9).While a large tidal volume relative to vital capacity does not necessarily indicate thatoxygen extraction will be large, a large oxygen extraction and a large tidal volume relativeto vital capacity will extend the respiratory interval significantly. These observationsappear to indicate a fundamentally different relationship among respiratory parametersthan that observed in terrestrial mammals, who breathe more frequently and do not extractas much oxygen as marine mammals (Stahl 1967, Schmidt-Nielsen 1990). While lung39volumes in marine mammals have been reported to be very similar to those of terrestrialmammals (Bryden 1988), tidal volumes at rest in these study animals are a larger fractionof the lung volumes compared to terrestrial mammals, resulting in a more completeexchange of respiratory gases. Tidal volumes in terrestrial mammals at rest are a smallfraction (1/6 to 1/7) of vital capacity (Schmidt-Nielsen 1984, 1990), but tidal volumes arehigher during exercise than during rest (Stahl 1967). This was not observed in killerwhales.While lung volume and oxygen uptake rates in killer whales are similar to thosepredicted by allometric equations established using data from terrestrial mammals (Stahl1967, Kleiber 1987, Bryden 1988), equations for respiratory variables should be used withcaution when applying them to mammals that have evolved specialized behaviours andphysiological adaptations for life in a marine environment.At night, the whales were observed to be in their calmest state and during rest hadlower respiration rates than those counted during the day in Activity state 1 (D.E. Bain,pers. comm.). The behaviour was very similar to that observed in Activity state 1, namelyhanging at the water surface, but the respiration rate was noticeably lower, and theduration of rest was longer.Bain (1986) and Ray et al. (1977, 1986) also noticed a reduction in respiration ratesduring night-time rest periods in other captive killer whales during 24-h respiration andbehaviour observations. Decreased respiration rates during rest periods in wild killerwhales have also been observed (Osborne 1986).Reasons for the increased respiration rates at rest during the day relative to night-time40are difficult to interpret, but one possible explanation is that the whales are in a differentemotional state once people are active around the pooi. Anticipation of feeding and showtimes may be one of the factors contributing to the elevated respiration rates observed inall whales, although the physical behaviour (hanging at the water surface) was the sameduring rest behavior at night and during the day.Apnea and Observed Rates of Oxygen ConsumptionInnes and Lavigne (1991) criticize Kasting et al. (1989) for not collecting consecutivebreaths from which to predict oxygen consumption. This criticism, of course, applies tothis study as well. Innes and Lavigne (1991) state that, as a result, Kasting et a!. (1989)were not justified in assuming that the relationship between oxygen consumption andapnea duration was determined in a steady-state, resting condition. They claim that theexpected relationship between oxygen extraction and apnea duration should be linear, andnot curvilinear as suggested by Kasting et a!. (1989) and as reported here.Using a large sample of respiration collections should eliminate the bias that couldoccur by collecting single respirations. The possibility of collecting data at a consistentbreath during the respiratory cycle, which is characterized by a sequence of breathsseparated by short apneas, followed by a single long apnea, should also be eliminated.Breaths were collected at a variety of points during the respiratory cycle, but it is notknown whether this eliminated the bias of collecting single breaths.Using Lenfant et a!. (1968) data on the partial pressure of oxygen in the lung atexhalation, and information on the basic chemistry cited by Peters (1983) that flux rate is41proportional to the partial pressure difference between the lungs and the blood, severalarguments can be proposed to show that the relationship between oxygen extraction andapnea duration is curvilinear in killer whales:a) When the whale inhales initially, there is a large difference in oxygen partial pressurebetween the lungs and the blood. As a result, the oxygen flux from the lung to theblood is high; andb) The high flux depletes oxygen in the lung which reduces the flux rate.Once the flux rate drops below that required to maintain the animal’s metabolic rate, theuse of oxygen stores in the body, such as in the muscle, would be initiated. This modelaccounts for the curvilinear and not linear nature of the data. Innes and Lavigne (1991)proposed a linear fit in which the intercept reflected the mean oxygen debt at the end ofapnea, and the slope reflected metabolic rate. However, the metabolic rate they inferredwould require nearly 120 s to build up the debt indicated by the intercept, whereasKasting et a!. (1989) and I found that mean apnea was approximately 60 s for Hyak, thelargest of my study whales. Thus attempts to fit a straight line such as proposed by Innesand Lavigne (1991) are unlikely to reflect the true relationship between oxygenconsumption and apnea.While, after any breath in the respiratory cycle, a decrease in the concentration ofoxygen in the lungs relative to atmospheric oxygen is experienced, most of the oxygendepleted air gets exchanged during the first breath. As oxygen diffuses into the blood, the42rate of oxygen flow from the lungs to the blood decreases as the gradient between theoxygen level in the blood and atmospheric oxygen declines.Regardless of the model chosen, over the range, of apneas tested there is little differencein the mean rate of oxygen uptake between the log-log model used in this study and alinear fit model with an appropriate intercept, such as that proposed by Innes and Lavigne(1991).Three trends can be interpreted from the oxygen extraction as a function of apneacurves:a) For a given apnea, oxygen consumption per ml of tidal volume is consistently higherat higher activity states.b) Within each activity state, oxygen consumption rate declines with an increase inapnea.c) The rates of oxygen extraction are higher immediately after a breath than are thoselater on; this trend was consistent for all individuals in all activity states.Oxygen consumption increased with increasing activity state. Hewlett (1970) reportssimilar results for Skana, a female killer whale of similar size to Vigga. Skana’s tidalvolumes ranged from 50 to 60 1 every 20 to 60 s. She consumed 3 to 4 1 of02/min atrest, and this increased to 9 1 of02/min at a mean tidal volume of 78 1. These oxygenconsumptions are the equivalent of 9.94 to 13.3 kcal/kg/day at 3 to 4 1 of02/min, and theanimal used 29.8 kcal/kg/day at 9 1 of02/min. This latter level was similar to Activitystate 3 in this study.43Estimated Standard Metabolic RatesTo allow interspecific comparisons among different species, the data in Activity state 1were collected as closely to Brody’s (1945) and Kleiber’s (1987) criteria as possible. Thesecriteria state that in order to collect comparable data on metabolic rates, the animals haveto be in a calm and relaxed physiological and psychological state, in a post-absorptivecondition and be placed in a thermoneutral chamber. Only healthy, sexually andphysically mature animals, neither pregnant nor lactating, can be considered. Hyak andYaka both fit these criteria, except that they were possibly not in the same calmpsychological state in which they were during night-time observations, hence theirrespiration rates were corrected to those observed during Activity state 0. The watertemperature in the pools in which the animals live is probably well within the animals’thermal neutral zone (Chapter 2 and see Williams et al.1991).Schmidt-Nielsen (1979) determined that the moving metabolic rate of terrestrialmammals rises in direct proportion to velocity for walking and running from a velocity ofalmost zero to maximum. The BMR is lower than the intercept of the regression linecalculated for the moving metabolic rate as a function of velocity. Schmidt-Nielsen(1979) called this metabolic rate at zero velocity the “basal metabolic rate plus posturalcosts” because the body needs to be held in an erect running position. Taylor et a!.(1970) approximated this as 1.7 times the basal metabolic rate. Metabolic rate in Activitystate 1 is approximately two times the basal metabolic rate and may reflect an analog topostural cost.Comparing the whales’ metabolic rates at night-time rest to Kleiber’s (1987) data it is44obvious that all the animals in this study except for Vigga have slightly higher metabolicrates than the terrestrial mammals investigated by Kleiber (1987).Kleiber (1987) predicts the basal metabolic rate of an animal Hyak’s and Yaka’s size tobe 25% and 16% lower, respectively, than was measured in this study. However, byusing oxygen consumption values from Activity state 1 and replacing respiration ratesfrom Activity state 0 it is likely that the resting metabolic rate was overestimated. It ispossible that not just the respiration rate was lower during Activity state 0, but the oxygenconsumption rate was lower as well.Taking Brodie’s (1975) and Lockyer’s (1981a, 1981b) arguments about using standard ormaintenance metabolism for cetaceans into consideration instead of estimating basalmetabolism, it is to be expected that killer whales’ standard metabolic rate might beslightly elevated relative to that of terrestrial mammals’ standard metabolic rates.Estimates of basal metabolic rates made by Kasting et al. (1989) using the sametechnique used in this study were more than two times higher than metabolic ratesestimated for the killer whales in this study. McAlistair (1981) estimated BIVIR for marinemammals of different sizes based on food consumption of captive cetaceans and alsosuggested higher metabolic rates than the estimates for killer whales in this study. Thevalues of these study animals’ standard metabolic rates are within the ranges predicted formammals and are even below that of a terrestrial mammal of comparable size. ComparingYaka’s SMR to that of an elephant (Benedict 1938) which is almost identical in size,shows that this killer whale has a metabolic rate (10.9 kcallkg/d) 18% lower than theelephant (13.3 kcal/kg/d). McNab (1986) states that BMRs of terrestrial carnivores45average 1.47 times Kleiber’s general prediction but this is not considered to differmarkedly from other mammals. Ridgway (1972) also states that a high protein diet alonecan contribute considerably to a high metabolic rate. Metabolic rates of the killer whalesstudied here can therefore be considered to be similar to those of other mammals.Kasting et a!. (1989) employed the same technique as used here for respirationcollection, but obtained substantially different results. Their estimated mass-specificmetabolic rates are 2.3 times higher than those determined in this study. Primary causes ofthe difference about standard metabolic rates were the activity state and the weight of theanimals. While Kasting et al. (1989) used respiration rates counted during the day, thisstudy exchanged reduced respiration rates observed during night time rest for respirationrates counted during rest periods during the day to estimate standard metabolic rates.Body weights in Kasting et al’s (1989) report are 23% lower than the weight for killerwhales used in this study. Minor differences exist in respiration rates during Activity state1, tidal volumes and possible oxygen uptake, and while two of the killer whales that heexamined were sexually mature, they were not physically mature (Duffield and Miller1988, Innes and Lavigne 1991). Brody (1945) found that the resting metabolic rates ofgrowing terrestrial mammals can be up to twice the BMR of adults. However, Kasting eta?. (1989) used the data from both mature and immature animals to develop a regressionequation predicting basal metabolic rates for differently sized killer whales.Estimated Daily Caloric ExpendituresThe two adult animals, Hyak and Yaka, had daily caloric expenditures which were46between 2.7 and 2.9 times those of the animals’ standard metabolic rates. This iscomparable to published data for terrestrial mammals, which has been estimated as 1.7 to3 times the basal metabolic rate (Wunder 1975, McNab 1980, Peters 1989). Other studieshave also yielded similar conclusions on pinnipeds’ average daily metabolic rates beingsimilar to those of terrestrial mammals (Kooyman et at. 1973, Lavigne et a!. 1982, Murie1987).Metabolic ScopeThe minimum estimates of metabolic scopes for the four killer whales studied are lowerthan those observed in terrestrial mammals which have a typical metabolic scope of 10(Hemmingsen 1960). Yaka had a respiration rate of up to 180 breaths/h during extremelyhigh activity, and Bain (pers. comm.) observed a minimum breathing rate of 24 breaths/hfor Yaka that occurred during what may have been sleep. This is a 7.5 fold increasebetween the lowest respiration rate observed during continuous rest and the highestsustained breathing rate ever observed in this individual. In addition, the measuredoxygen consumption per breath and unit time increased with activity. However, standardmetabolic rates may have been overestimated by using the oxygen consumption measuredin Activity state 1 and using only respiration rates collected during Activity state 0.Similarly, using oxygen consumption determined during Activity state 3 and respirationrates counted during Activity state 4, may have underestimated maximum metabolic rate ifoxygen consumption rates were higher during Activity state 4 than during Activity state 3.While an approximate metabolic scope can be obtained by using the above mentioned47method using both respiration rates and caloric expenditures, ranging from 1.4 to 7.5,maximum exertion was most likely never reached because the whales were not pushed totheir maximum limits during and after shows. These metabolic scopes estimated for killerwhales are slightly higher than Irving et al.’s (1941) and Irving’s (1973) estimates thatbottlenose dolphins (Tursiops truncatus) may not increase their oxygen consumption tomore than three or four times their resting rate. Irving et a!. (1941) and Irving (1973)describe aquatic mammals as having a high metabolic rate compared to other mammalsand a modestly expanded metabolic rate for daily activities; he states that marinemammals have little scope for an increase in tidal volume and the degree of oxygenutilization. While metabolic scopes in this study were higher than those reported byIrving et a!. (1941) and Irving (1973) for bottlenose dolphins, they were lower than thoseobserved in terrestrial mammals. A better understanding of how oxygen uptake rates varywith activity rate as well as pushing the whales to their maximum limit would be neededto accurately determine metabolic scopes.Difficulties and ReliabilityThe most questionable factor in the respiration analysis was the determination of tidalvolumes. This is because the researcher can not be certain whether the animals exhalednormally. While Hyak, Finna and Yaka adapted well to the breathing apparatus, it wasclear that Vigga did not. One important factor in the difference of her data to those of theother whales is that her tidal volumes are low because she did not exhale fully. While nodata from Vigga or any of the animals were used where they exhaled again instead of48inhaling after breath collection, it was the strong suspicion of myself, the training staff andother research personnel that Vigga did not exhale fully with the apparatus on herblowhole. As a result, her metabolic rate tested by respiratory analysis may beunderestimated by an unknown amount. It is also unknown how uniform tidal volumesare during normal breathing as well as how uniform the extrapolated oxygen uptake ratesare because respirations were requested after predetermined apneas.Some uncertainties existed in the estimated weights of the animals. Weighing theanimals on a regular basis at the 2 aquaria where the studies were conducted would add tothe knowledge of growth of killer whales in aquaria.While activity budgets were observed during the study, they change on a daily basisand hence determination of activity budgets would have to be repeated during furtherstudies.49Chapter 2: FOOD CONSUMPTION AND THE iNFLUENCE OF OTHERFACTORS ON FOOD INTAKE IN CAPTWE KILLER WHALES, Orcinus orcaINTRODUCTION AND OBJECTWESEstimates of food intake are fundamental to the study of the ecology of any animal.Direct measurement of food intake by wild cetaceans is difficult because the animalsgenerally feed under water and out of sight. This chapter was designed to comparerespiration-based estimates of energy expenditure of captive killer whales (Orcinus orca)(Chapter 1) to the food intake by those whales in captivity at the time of the respirationmeasurements.In addition, long term food records were evaluated for possible factors affecting foodintake. Factors affecting food intake in killer whales and other species may includegrowth, reproductive status, health, water temperature, ocean of origin and time of year.Caloric intake can be calculated based on the amount and type of food provided. Thistogether with estimates of body size of the animals can be used to develop formulas thatcan be used to estimate food intake as a function of body size.Studies on food intake of captive cetaceans have been conducted on several species byanalyzing daily food records and relating food intake to growth and estimated weight ofthe animals. Kastelein and Vaughan (1989) determined the daily food consumption of acaptive female Atlantic killer whale by analyzing daily food records and relating food50intake to growth and estimated weight of the animal. This whale consumed 7% of herbody weight per day as a 1-year old calf at 315 kg which decreased to 2.1% of her bodyweight of 1900 kg as a subadult. Two smaller, sub-adult male killer whales (4.67 m long,1040 kg; and 4.9 m long with a calculated weight of about 1500 kg) consumed 4.3% and3.9%, respectively, of their body weight on a daily basis (Sergeant 1969).Captive growing beluga whales (Deiphinapterus leucas) weighing around 200 kgconsumed 4.5% of their body weight per day, which was reduced to 1.2% in adult animalsweighing 1400 kg (Kastelein et a!. 1994).Adult Commerson’s dolphins (Cephalorynchus coniinersonhi) weighing between36 to 43 kg were observed to consume between 9 and 12% of their body weight per day(Kastelein et a!. 1993). Adult male harbour porpoises (Phocoena phocoena) weighingbetween 32 and 40 kg ate approximately 8% of their body weight per day, while growinganimals (16 to 24 kg) consumed 10.4% to 13% of their body weight per day (Andersen1965, Kastelein et al. 1990).These studies show that small species and young cetaceans typically eat more inrelation to their body weight than do large cetaceans. This was confirmed by Sergeant(1969) who reported feeding rates of eight different odontocete species in captivity. Hedetermined that body weight was inversely proportional to food intake as a percentage ofbody weight.As indicated by the above studies, body weight is important in determining food intake.Based on empirical data Bigg and Wolman (1975) developed the following equation toestimate body weight of killer whales:51[13] M = 0.000208 L2577,where M is body mass in kg and L is total body length in cm.Mean length at birth for killer whales in British Columbia (based on stranded neonates,n=6) is 244 cm (Bigg 1982). In the North Atlantic, newborns are on the average 213 cmin length (based on whaling records, n=5, Jonsgard and Lyshoel 1970). Growth rates ofyoung killer whales in aquaria average 37-38 cm/y (Bigg 1982, Duffield and Miller 1988).After reaching approximately 488 cm in length, growth rate declines in both sexes, withthe females ceasing growth at about 580 to 600 cm body length, while males may growup to 900 cm in length before growth ceases (Reeves and Mitchell 1987).Bigg (1982) concluded that data from animals in captivity provided a guide to potentialgrowth rates of wild killer whales, but suggested that captive animals grow faster thantheir counterparts in the wild. Based on captive growth rates, length at sexual maturitywould be reached by 7 y of age, but observed ages of maturity in the wild range from 11to more than 15 y (Bain pers. comm., Bigg et a!. 1990, Olesiuk et a!. 1990). Asper et a!.(1988) report a length of 400 cm for a 28 month old Atlantic-Pacific hybrid female calf,indicating growth rates in aquaria are enhanced compared to growth rates in the wildwhere a young killer whale would be approximately 315 cm at that age.Another factor reported to influence food intake is water temperature. Williams et al.(1991) studied the thermal limits of captive bottlenose dolphins by measuring theirmetabolic rate. The dolphins maintained a stable body temperature in water ranging from3.6 °C to 17.3 °C, while their metabolic rate was stable between 6 °C and 16 °C. The52thermal neutral zone of killer whales is not known, but the species inhabits the coldwaters of the Arctic and Antarctic as well as the warm waters of the equatorialconvergence zones (Heyning and Dahiheim in press). Water temperatures between thecold arctic waters and warm equatorial currents range from -1.3 °C to 27°C (Sverdrup eta!. 1946). To maintain a constant body temperature in varying water temperatures, killerwhales, and cetaceans in general, have developed many adaptations, such as countercurrent heat exchange (Bryden 1988), integument modifications (Ridgway 1972),restriction in body surface area, and respiratory modifications (Gaskin 1982). Phenotypicadaptations include variations in blubber thickness and blubber lipid levels (Williams1991, Worthy 1991). Worthy and Edwards (1990) and Worthy (1991) showed that whilecetaceans exhibit seasonal changes in blubber thickness, presumably in response to watertemperature changes, there are also data from five species of dolphins to suggest that thelipid content of the blubber layer changes with season, ranging from 30 to 95%. Dramaticregional and seasonal variations in lipid content in bottlenose dolphins was also observed(Worthy 1991). Therefore, both the quantity and quality of the blubber layer can change,and are important for thermoregulation in dolphins.A seasonal decrease in food intake with increases in water temperatures was observedin captive Commerson’s dolphins held at five different aquaria (Kastelein et a!. 1994).Food intake in captive beluga whales (Deiphinapterus leucas) is negatively correlated withwater temperature, with food intake decreasing approximately 30% during warmer summermonths (Kastelein et a!. 1994). This decrease in food intake corresponds to the same timethat wild beluga whales reduce their food consumption due to migration. Perhaps internal53factors rather than lowered heat loss reduce food intake of belugas during this period(Kastelein et a!. 1994).Pregnancy and lactation increase food intake in most mammals including captivecetaceans. While food intake increased only slightly during the last month of pregnancyin bottlenose dolphins, increases in food consumption of 129% to 204% were foundduring lactation (Reddy et a?. 1991). No increase in food consumption was found duringpregnancy in Commerson’s dolphins, but food intake in these animals increased by 30%during lactation (Kastelein et a?. 1994). Food intake in beluga whales increased duringlactation by up to 100% (Kastelein et a?. 1993).It has been questioned in the past to what degree food intake in captivity reflects foodintake in the wild. Aquarium staff today take into consideration the overall appearanceand motivation of the animals toward food, and generally feed the animals to satiation.Studies of terrestrial mammals (Brody 1945, Kleiber 1987) have shown that not all foodingested can be metabolized and used by the animal. To compare energy expenditure tofood consumption, food intake needs to be corrected for urinary, fecal and respiratorylosses. Net assimilation efficiency (NAE), the ratio of absorption to ingestion (Peters1983), was reported to range from 67.7% to 74.6% in adult harp seals (Pagophilusgroenlandicus, Lavigne et a?. 1982). Worthy (1990) cites studies determining NAE’s fordifferent species of pinnipeds ranging from 88% NAE after pollock (Pollachius virens) to97% after herring (Clupea harengus) consumption. Assimilation levels for mackerel(Scomberjaponicus) consumed by Black Sea bottlenose dolphins (Tursiops truncatus)were 89% to 90% (Shapunov 1973 a and 1973b). A value of 74% for NAE was54suggested for metabolic rates of harbour porpoises, Phocoena phocoena (Yasui and Gaskin1986). Lockyer (1981a, 1981b) estimated this correction factor to be between 70% and80% for blue (Balaenoptera musculus) and sperm (Physeter catadon) whales.In this chapter, the determination on how closely daily energy expenditures estimatedby respiration analysis in killer whales (see Chapter 1) match the animals’ observed foodintake in the aquarium, is described. Such comparisons of measurements of food intakeand metabolic rate studies by indirect calorimetry have not been reported before forcetaceans. The food intake data of the same four killer whales studied in Chapter 1 formetabolic rates determined by respiration analysis and two additional individuals werecollected.The objectives were to:1. determine the quantity of food killer whales were fed in a captive environment;2. determine any differences in food intake within and among individual whales andidentify factors related to food intake;3. compare food consumption to energy expenditure estimated from respiration analysis(data from Chapter 1); and to4. estimate net assimilation efficiency.55METHODSAquarium personnel at two aquaria have recorded the daily food consumption (speciesof fish and amount fed) by six killer whales held at two aquaria. Combined, these dataamount to a total of 80 whale-years (where data from one whale for 1 year = 1 whaleyear, Bigg 1982). Each whale’s arrival date, size and estimated age at capture and yearsfor which food data were available are summarized in Table 15. In addition, availablerecords of daily water temperatures, reproductive, and health status, together withinterviews with the training staffs were used to examine variations in food intake.While some of the factors such as the amounts of food consumed can be statisticallyanalyzed, others, such as comparisons between aquaria, can only be described because ofthe small number of independent samples in this study.Age EstimationThe ages of the individual whales at the time they were captured were estimated asfollows:[14] age (y) = [length at collection (cm) - length at birth (cm)] I growth rate + D (y)where: length at birth was assumed to be 244 cm for killer whales from British Columbia(Bigg 1982) and 213 cm for whales from Iceland (Jonsgard and Lyshoel 1970, Duffieldand Miller 1988). Growth rate is estimated at 37 cm/year up to a length of 488 cm forboth Pacific and Atlantic killer whales, and D is the estimated difference in growth of56Table15. Descriptionsofthestudyanimalsandavailabilityoffoodrecords.AnimalSexDateOceanInstitutionLengthEstimatedYearsFoodCollectedOfOriginMeasuredYearAtDataAtOfAquariumAvailableCaptureBirth(cm)SkanaF2/67PacificVA*43919611967-19801967-19691971-1980HyakM4/68PacificVA*30419671968-19911968-19691971-19841986-1991FinnaM11/80AtlanticVA*39419751980-Present1981-19841986-1993BjossaF11/80AtlanticVA*40419741980-Present1981-19841986-1993YakaF12/69PacificMWA/USA**32019671969-Present1983-1993ViggaF11/80AtlanticMWAIUSA**32019771980-Present1983-1993*VancouverAquarium, Vancouver,B.C.**MarineWorldAfrica/USA,Vallejo,CAwild and captive whales (Asper et al. 1988). D was set to one year added for all whalescoming into captivity after 5 y of estimated age, to correct for the assumed slower growthof the animals in the wild during the first years of rapid growth in killer whales (Bigg1982, Asper et a!. 1988).WeightThe captive animals used for this study had been measured for length (Figure 11) atvarious time intervals (Table 16). These data were used to calculate weights for theindividual animals (Table 16) using Bigg and Wolman’s (1975) equation for therelationship between body length and weight. For all weights, except the first one foreach animal, 20% extra body weight was used for each whale (see Chapter 1).Food Data CollectionAquaria food records date back to 1967 and were collected through 1993. Twoindividuals (Skana and Hyak) died at the Vancouver Public Aquarium, and for bothindividuals most food data from the time of their arrival to their deaths were available.The other animals studied were still alive as of 31 December 1993 after which data arenot included here.Food records were entered on a daily basis by the training personnel except for Finnaand Bjossa during 1991 to 1993, when food data were entered on a weekly basis.Continuous food consumption data were not available for all individuals because of datalost by the aquaria. All available data were used. These data were entered into a588007002001100 0IIIIIIIIIIIIIIIIIIIIII051015202530Age(Y)—m—Skana—V--Hyak——Finna——Bjossa—s—Yaka—a—ViggaFigure11.Relationshipof bodylengthtoageofsixkiller whales.Table 16. Estimated weight of six killer whales based on their length.Animal Year Length EstimatedOf WeightMeasurement (Bigg andWolman 1975)(cm) (kg)Skana 1967 439 13411968 472 16171969 500 18761970 508 19551971 551 24101974 554 24441980 577 2714Hyak 1968 304 5211969 345 7211970 394 10151971 455 14711974 531 21911976 572 26541977 612 31591980 660 38371987 665 39131991 716 4733Finna 1980 394 10151981 396 10291984 472 16171986 564 25591987 584 2800Bjossa 1980 394 10151981 404 10831984 404 10831986 505 19251987 531 2191Yaka 1969 320 5941993 584 2800Vigga 1980 320 5941993 513 200560spreadsheet (Quattro Pro), and were separated by species fed and with the correspondingquantities fed. The majority (>60%) of fish fed was herring (Clupea sp.) with theremainder consisting of mackarel (Scomber sp.), smelt (Osmeridae), capelin (Mallotusvillosus), salmon (Salmonidae), and cod (Gadus sp.). The combination of fish fedchanged slightly on a daily basis depending on the availability of fish. Each food specieswas assigned a caloric value (Perez et a!. 1990) and all different daily items were summedto estimate the total amount fed in kcal/day.Yearly food consumption was graphed by age and sex to compare among individuals.Pregnancies were noted in the records and used to examine the effect of reproductivestatus on food intake.Urine Collection and Net Assimilation EfficiencyAttempts were made to collect urine from three female killer whales (Yaka and Viggafrom Marine World and Bjossa from the Vancouver Public Aquarium). The animals weretrained to provide urine samples which were analyzed via the Kjeldahl method (AOAC) todetermine urinary nitrogen content (Brody 1945) and correct the total amount of foodconsumed for the amount of food actually absorbed from the gastrointestinal tract (NAE).However, because it was logistically impossible to collect the total amount of urine andfeces excreted throughout the day, these data could not be used to correct for assimilationefficiency. The net assimilation efficiency was estimated as the number of calories burned(Chapter 1) divided by the estimated number of calories consumed by the individual whaleduring the period of time when the respiration study was conducted.61GrowthThe daily growth (kg) was calculated from the estimated weights (Bigg and Wolman1975) based on length of the animals (Table 16). The energy required for weight gainwas calculated based on the combustion of weight gain of 5971 kcal/kg (Blaxter 1989).STATISTICAL ANALYSESa) Temporal Variation of Food ConsumptionMonthly averages of food consumption were calculated for each whale. A two-wayanalysis of variance was performed to test the significance of variation in food intakebetween months and between years. Because pregnancy and lactation can affect foodconsumption, data for Bjossa were analyzed both as a complete data set and with datafrom the gestation and lactation period removed to compare her to other females whowere not pregnant.b) Variation in Food Consumption Between IndividualsIntrasex comparisons were made among the whales to determine possible individualdifferences in food consumption when the animals were compared at the same age.Regression analyses were performed to determine the relationship between the food intakeof two different individuals of the same sex at the same age. Paired two-sample t-testswere performed, comparing the annual average of food intake matched for age and todetermine if the animals on average consumed the same amount of food at the same age.62Paired tests were used because of the increased power of the test. Due to the smallsample size a Mann-Whitney U test was used to determine if differences exist betweenYaka and Bjossa.c) Water TemperatureLinear regressions of daily food intake versus water temperature were calculated forYaka and Vigga from 1986 to 1993. Water temperature data from the Vancouver PublicAquarium were available only for 1993, hence linear regressions were calculated for Finnaand Bjossa for that year only.d) Reproductive StatusThe daily food intake during Bjossa’s pregnancies and the peaks of food intake duringlactations were compared to the average food consumption for the same months during theyears prior to giving birth. These comparisons allowed the examination of changesassociated with her reproductive status.Food Consumption Relative to Body WeightAverage food intake was divided by body weight to estimate food intake in kcal/kg/day.The Nonlin function of Systat was used to calculate the best fit equation of the form:[15] Food Intake (kcal/day) = amb,where a and b are constants and m is body mass in kg (Peters 1983).63Determination of Net Assimilation EfficiencyData on food consumption were compared to energetic expenditures calculated fromrespiratory analysis for Hyak, Yaka, Finna and Vigga. Net assimilation efficiencies werecalculated independently for each one of the four whales to match food consumptioncorrected for NAE to the daily energetic expenditure estimated from respiration analysis.RESULTSFood Consumption and Individual Variation in Food IntakeFood intake on a yearly basis between the two individual males and the four individualfemales controlled for age was compared (Figures 12 and 13). Statistical comparisonscould not be made between Vigga and Yaka because data were unavailable where agescould be matched (see Figure 13). Regressions and t-tests analyzing variation amongindividuals in food intake of the two males and among the four females matched by ageshowed no consistent trends (Table 17). Food consumption as a function of age washighly correlated for the two males. While the correlation of food consumption as afunction of age for the two female Pacific whales was weak, the animals also ate verydifferent amounts of food. Although food consumption as a function of age was highlycorrelated comparing the Icelandic females, Vigga’s food intake was consistently greaterthan Bjossa’s. There were low correlations for food intake as a function of age comparingIcelandic versus Pacific whales, even though the amount of food consumed was similar.64120250000a—100----k--A2000O0V——0—A60100000AFoodIntake(kg/d)=3.75age+16.8V20Ar=O.89,n33,p<O.OOi,SE=24500000IIIIIIIIIIIIIIIIIIIII016111621AGE(Y)HYAKAFINNA1Figure12.Dailyfoodconsumptionbymalekiller whales.908O‘7O-0 0 i4o 302O.1o 0ON200000180000160000140000120000100000800006000040000200000C)AGE(Y)LBJOSSAoSKANA•VIGGAvYAKAFigure13.Dailyfoodconsumptionbyfemalekiller whales.Table17. Individual variationinfoodintakeamongsixcaptivekillerwhales.Regressionanalysisshowingtherelationshipbetweenfoodintakeof2differentindividualsmatchedforsexandage.Paired2-samplet-testshowingwhethertheannualfoodintakefor 2whalesmatchedforageandsexarethesame.*all tests=Studentst-test,except(u)Mann-WhitneyUtestAnimalsCompared#of Yearsr2Significancet-valueSignificanceHyakandFinna120.86p<0.001I1.87p>0.08BjossaandVigga90.73p<0.01I2.66p<0.02SkanaandYaka50.05p>0.5I3.91p<O.OlSkanaandVigga90.1p>0.20.02p>0.98SkanaandBjossa110.06p>0.2I1.98p>0.07YakaandBjossa(u)4--I-p<0.05Factors Related to Variation in Food Intakea) Temporal Variation of Food Intake within IndividualsAnalysis of temporal variations in food consumption (Table 18) shows that food intakeof both males differed significantly both by month and by year. For all females exceptBjossa, food consumption was not significantly different on a monthly basis. Annualvariation was significant for all females.b) Water TemperatureDaily food intake was compared to water temperature ranging from 7 °C to 23 °C forthe two whales at Marine World from 1986 to 1993. The total of 2,724 d for which bothfood consumption and water temperature data for Yaka were available (Figure 14) and2,727 d of water temperature and food consumption data for Vigga (Figure 15) wereplotted. There was no relationship between food intake and water temperature for eitherof the two whales (r2 = 0.0004, and r2 = 0.00026, respectively).However, food intake as a function of water temperature for Finna showed a negativecorrelation (r2=0.34 and p<O.OOl, Figure 16). Over the range of temperatures observed (7to 19 °C) this reflects a range of 14.27 kg or ±9.2% of food intake (1.25 kg 1°C). A t-test(Zar 1984) was performed to determine that the slope of the regression line wassignificantly different from 0 (t = 13.74, p < 0.001). For Bjossa, regression analysis alsodetermined a negative slope (p<O.OO1 andr2=0.15 ). A range of 3.04 kg or ±3.27% (0.27kg I °C) of food intake was observed with a change in water temperature. This slope issignificantly different from 0 (t 7.99, p<O.OOl), although the magnitude is small (Figure 17).68Table 18. Temporal variation of food consumptionby month and year for six captive killer whales.NS = not significantMonthly YearlyWhale Variation VariationSkana NS p<O.OO1F=O.70 F=18.46df=11 df=lOHyak p<O.OO1 p<O.OO1F=4.99 F=85.13dfll dll18Finna p<O.OO1 p<O.OO1F=2.73 F=211.29df=11 df=11Bjossa p<O.Ol p<O.OlF=2.90 F=4.69d1=11 df=5Yaka NS p<O.OO1F=O.87 F=8.84df=11 df=9Vigga NS p<O.OO1F=O.59 F=58.Odf=l1 df=869Figure 14. Food intake for Yaka as a function of water temperature.1008060z402005 10 15 20WATER TEMPERATURE (DEGREES C)25Figure 15. Food intake for Vigga as a function of water temperature.70100T+No80860 ----------004020-0 I I I I I I I I I I6 8 10 12 14 16 18 20WATER TEMPERATURE (DEGREES C)Figure 16. Food intake for Finna as a function of watertemperature, 1993.60::30 - ........ -820 -10 -0 I I I I I I I I6 8 10 12 14 16 18 20WATER TEMPERATURE (DEGREES C)Figure 17. Food intake for Bjossa as a function of watertemperature, 1993.71c) Reproductive StatusThe yearly food consumption by Bjossa was plotted for the two years (1988 and 1991)in which her calves were born (Figures 18 and 19). While data from the first pregnancyindicate no increase in food consumption before the 1988 calf was born, Bjossa increasedher food intake steadily by a total of 25% one month before the second calf was born.After giving birth, Bjoss&s food consumption increased by 100% from pre-parturitionamounts for the first calf and 60% for the second calf (Figures 18 and 19). In both casesfood consumption fell to normal levels within 8 and 16 d, respectively, after the calvesstopped nursing.GrowthDaily growth rates ranged from 0 kg to 1.29 kg which corresponds to a maximum of7,700 kcal/d used for growth. Calories required for growth were negligible relative to thetotal food intake (see Figures 12 and 13).Food Consumption Relative to Body WeightFood intake as a function of estimated body weight is shown in Figure 20 and is alsoshown as a fraction of body weight in Figure 21 and yielded the following equation forfood intake by killer whales:[161 Food Intake = 0.277 M°663 (r20.76, df=78, p<O.OO1, SE=0.042),where food intake is in kg/d and m = body mass (kg).72120calfI diedj:I I I I I I I I I I IFigure 18. Food intake for Bjossa during pregnancy and lactation, 1988.Figure 19. Food intake for Bjossa during pregnancy and lactation, 1991.10011‘2)c 60402000 30 60 90 120 150 180 210 240 270 300 330 360Day of YearcalfseparatedIIIIIIIIIIIIIIII12010080c 60402000 30 60 90 120 150 180 210 240 270 300 330 360Day of year731000CINTM = 0.277 MASS°6631 I I I I I liii I I I I liii100 1000 10000BODY MASS (kg)Figure 20. Food intake as a function of estimated body mass in six killer whales.0.060.05 .._. ...... .. ... ... ......0E-0.01 ............ - ... ........z0 0 I I I I I I I I I0 1000 2000 3000 4000 5000 6000BODY MASS (kg)L SKP,NA V HYAK 0 HNNA BJOSSA • YAKA A VIGGAFigure 21. Food intake as a fraction of estimated body mass in six killer whales.74Statistics on the log-transformed data showed that the slope of the line was significantlydifferent from 0 (p<O.OO1).Food intake by males declined from 5.3% to 1.3% of their estimated body weight perday as the animals were growing from a 1-year old to adulthood, and females’ foodconsumption declined from 2.6% to 1.3% of their estimated body weight while growingfrom 3-year old juveniles to adults (Figure 21).Net Assimilation Efficiency and Daily Caloric Consumption vs. Daily Caloric ExpenditureNet assimilation efficiencies calculated for food intake for each whale were matched tothe energy expenditure measurement by respiration analysis as closely as possible. Forthree out of the four whales (Hyak, Finna and Yaka), the net assimilation efficiencyranged from 0.80 - 0.83 (Table 19). Vigga’s NAE was estimated at 0.46 (Table 19). Thisstands in contrast to the other whale’s and reports of NAE’s for other marine mammalscited in the literature which report that NAE’s for fish eating marine mammals isconsistently high (>67%). The mean NAE for all four killer whales was calculated at 0.73.75Table19.Comparisonbetweendailyenergeticexpendituremeasuredbyrespirationanalysisandfoodintakeinfourcaptivekillerwhales.Foodintakewascorrectedindividuallyfornetassimilationefficiency(NAB)tomatchtheestimatedenergyexpendituresbasedonrespirationanalysis.EstimatedEnergyFoodIntakeNABRequiredtoMatchExpenditurebasedonFoodIntaketoRespirationAnalysisEstimatedEnergyExpenditurefromRespirationAnalysiskcal/daykcalldayHyak141,600170,0000.83Finna88,301110,0000.80Yaka107,669130,0000.83Vigga50,891110,0000.46DISCUSSIONFood Intake and Individual Variation in Food ConsumptionNot surprisingly, food intake varied among individuals and within an individual at agiven age. The sample of four females and two males is too small to statisticallydetermine whether variation of food consumption was affected by factors such as sex,aquarium, or ocean of origin, or simply reflected individual differences. Although animalsin both aquaria were fed to satiation, individual differences appear to be a factor in foodintake. It will be necessary to include and perform analyses of more food records of killerwhales and more institutions holding killer whales before the effects of individualvariation and institutions on food consumption can be ascertained. It did appear that allanimals showed a significant difference in year to year variation in food intake. This is tobe expected because the animals were growing during much of the period over which thedata were recorded. While the food species fed in the aquaria is similar to those found tobe consumed by wild killer whales in the Atlantic with the majority of food being herring(Christensen 1984), the prey items for wild Pacific killer whales consists mainly of salmonwith a smaller percentage of other fish species during spring, summer and fall, and avariety of fish species during the remainder of the year (G. Ellis, pers. comm.). For thatreason, caloric values of fish fed to the whales should be determined rather than justreporting the amount of food (kg) consumed by the whales.77The best fit for food intake rate as a function of body weight for the six different killerwhales:[17] Food Intake = 0.277 Mass°663,is similar to Innes et al. ‘s (1987) equation[18] Food Intake = 0.258 Mass°69,describing the feeding rates of a variety of immature and mature cetaceans.Body weight is correlated with food consumption. This inverse relationship betweenfeeding rate per unit body weight and body weight is what is expected from what hasbeen shown in terrestrial mammals and by the relationship between basal metabolic rateand body weight (Brody 1945, Schmidt-Nielsen 1990).Water TemperatureThere was no correlation between water temperatures and food intake for the twofemale killer whales at Marine World. Although there was a negative correlation betweenthese two factors for two whales from the Vancouver Public Aquarium, the magnitude wassmall. This difference could be due to several factors:a. The temperatures experienced in the two aquaria are well within the range of78temperatures experienced by the species in the wild and the water temperatureswere likely within the thermal neutral zone of killer whales. No or very littlechanges in food intake were observed.b. Changes in activity levels or in body weight may cancel out changes in heat loss. Thetwo killer whales at Marine World have a heavier performance schedule with moreshows during the summer, so increases in food intake required for higher activitylevels may cancel out the effect of increased water temperature on food consumption.c. Trainers at the two aquaria have different criteria for feeding the whales. It is only inthe last 5 y that feeding to satiation was really practiced consistantly at the VancouverAquarium (Jeremy Fitz-Gibbon, pers. comm.).Reproductive StatusNo marked increase in food intake occurred during Bjoss&s first pregnancy, it onlyoccurred during the last month of her second pregnancy. An increase in foodconsumption late in pregnancy has been reported in captive Commerson’s dolphins andbeluga whales (Kastelein et.al. 1993, 1994), bottlenose dolphins (Reddy et.al. 1991) and asmall increase in food consumption has been theorized for sperm whales (Physetercatadon) during the latter part of pregnancy (Lockyer 1981b).Bjossa’s food consumption increased by 100% after the birth of each calf. Thisincrease in daily food intake has been recorded for other cetaceans held in aquaria, suchas bottlenose dolphins (Reddy et al.1991) and beluga whales (Kastelein et.al. 1994) aswell as in pinnipeds (Perez and Mooney 1986). These data support Kastelein et al’s.79(1994) theory that gestation does not impose a marked energy load until the last stages ofpregnancy, while a large energy demand is seen during the first part of lactation. Bjoss&sfood intake decreased to normal levels within 8-16 d after she stopped nursing.Comparison between Caloric Intake and Caloric Expenditure and Net AssimilationEfficiencyThe results of the comparisons between caloric intake and caloric expenditure for thewhales were very similar to each other for 3 out of the 4 whales (Hyak, Yaka and Finna).Their individually calculated net assimilation efficiencies (80% - 83%) only vary by 3%.These NAE’s fall well within the reported range of NAE’s for fish-eating marine mammals(NAE between 0.67 to 0.93, Shapunov 1973, Lockyer 1981a, 1981b, Lavigne 1982,Worthy 1990). Vigga’s NAE is considerably lower than those of the other three whales.Her NAE (0.46) is also well below NAEs reported in the literature for fish eatingmammals (> 0.67). The reason for her low NAE is that her caloric expenditure is muchlower than her food consumption, possibly due to her dislike for the funnel (see Chapter1).This comparison between determining energy expenditures of three killer whales byrespiration analysis and verifying the data by looking at food intake indicates thatrespiration analysis is a consistent method and valuable tool for estimating metabolic ratesof most, but not all, captive killer whales.80Chapter 3: COST OF TRANSPORT, DRAG AND REALIZED METABOLIC RATEESTIMATES IN FREE-RANGING KILLER WHALES, Orcinus orca.INTRODUCTION AND OBJECTIVESAn individual’s energetic demands depend on its minimal metabolic rate [which can bethought of as the energy to maintain necessary life functions as defined by Brody (1945)and Kleiber (1987)1, plus energy associated with locomotion, thermoregulation, andproduction energy necessary for growth and reproduction (Wunder 1975, Gaskin 1982,Lavigne et al. 1982, Peters 1989). The animal’s minimal metabolic rate, the basal, orstandard, metabolic rate, can be estimated fairly accurately for generalist species notadapted for specialized conditions requiring elevated or reduced metabolism. Regressionequations established by many (Brody 1945, Hemmingsen 1960, Kleiber 1987, Peters1989; see also Chapter 1) are generally used to relate the metabolic rate to the animal’sbody weight. Realized metabolic rates, or the average daily metabolic rates, aredetermined in large part using data on animal activity (Peters 1989). The focus of thispaper will be on the locomotion component of realized metabolic rate in killer whales(Orcinus orca), which can be a significant fraction of the total energy used by an animal(Prange and Schmidt-Nielsen 1970, Gaskin 1982, Peters 1989).A common method to determine the energy necessary for locomotion is to measure thecost of transport (COT; the amount of energy necessary to move a unit of mass a givendistance) of an animal at different velocities including its minimum cost of transport81(Schmidt-Nielsen 1972, Tucker 1975) and its maximum range speed (Williams et a!.1993). For captive terrestrial mammals, COT is determined by measuring oxygenconsumption and body temperatures while at rest and while running on a treadmill atvarious speeds (Taylor et a!. 1970). The amount of energy expended above the energythat the animal uses for its basal or standard metabolic rate represents the increase in themetabolic rate due to locomotion.Since it is difficult to measure COT on free-ranging animals directly, an indirectmethod of calculating energetic cost in the case of swimming in cetaceans has beendeveloped. Swimming velocities and respirations are measured per unit time on free-ranging marine mammals, and tidal volumes and oxygen consumption are measured oncaptive animals or obtained from respiratory allometric estimates (Gaskin 1982).Measuring COT indirectly has been applied to several species of marine mammals. Theswimming metabolism of harbour seals (Phoca vitulina) was studied by placing theanimals into a flow channel and having the seals swim at different velocities by adjustingthe flow velocity of the water (Davis et a!. 1985). Oxygen consumption and carbondioxide production were measured to determine the cost of transport at differentswimming velocities. Standard metabolic rates were defined by having the seals rest instill water. Hydrodynamic characteristics and swimming performance were also measuredin harbour seals and demonstrated the importance of streamlining in this species todecrease their cost of transport during swimming (Williams and Kooyman 1985). Cost oftransport by swimming sea otters (Enhydra lutris) was determined by measuring oxygenconsumption and carbon dioxide production in captive individuals and analyzing82swimming modes and preferred velocities from videotapes of otters swimming in poois(Williams 1989).Other techniques for estimating the cost of locomotion in marine mammals have beenbased on measures of actual weight loss in large cetaceans. Energy expenditures inmigrating mysticetes were estimated from body weight difference due to the combustionof fat before and after the migration (Rice and Wolman 1971). Weight loss was thencalculated as a function of oxidation of fat, equated to energy requirements and theanimals’ cost of transport was estimated. Similarly, COT in fin whales (Balaenopteraphysalus) was inferred by measuring the difference in the amount of whale oil before andafter migration (Kawamura 1975). Kawamura (1975) extrapolated COT for the whalesfrom results of the cost of locomotion in salmon and based his calculations on having theanimal experience laminar flow of water around its body.The cost of transport in migrating gray whales (Eschrichtius robustus) was estimated bymeasuring swimming velocities and breathing rates. These data were combined withextrapolations of tidal volumes and oxygen consumption measured on unrestrained wildcalves and a captive gray whale calf to estimate the minimum COT (Sumich 1983).An estimate of COT and realized metabolic rate can also be obtained from theoreticalcalculations on hydrodynamics in cetaceans. A simple calculation permitting anapproximate assessment of streamlining is the fineness ratio (FR) which describes therelationship between body length and its maximum thickness. This dimensionless numberindicates to what degree a body approaches the optimal hydrodynamic shape (Gaskin1982). A fineness ratio of 4.5 is optimal for creating minimal drag for a given body83volume (Webb 1975, Feldkamp 1987). Cetaceans have developed several adaptations tominimize drag (drag is the pressure times the area, and the drag on an object is the netpressure across its projected area times that area [Vogel 1988]) and to delay turbulent flowuntil a higher swimming velocity. These adaptations include streamlining with theelimination of unnecessary protruding parts that would offer resistance to the water (suchas external ear pinnae, protruding mammary glands or reproductive organs, and hair) and apowerful tail to propel the animals through the water (Gaskin 1982, Evans 1987, Bryden1988). Despite these adaptations, even a streamlined cetacean has to overcome drag.Water provides resistance against movement and drag develops at the skin surface as theanimal moves through the water.Gray (1936) described experiments with a rigid dolphin model. These experimentsindicated that the power required to overcome the drag the animals experienced duringswimming was greater than the maximum power available from the locomotor muscles(Grays paradox). According to physical calculations, the animals would have toexperience mostly laminar flow around the body to be able to sustain the observedswimming velocities. While rigid bodies towed at velocities measured in swimmingcetaceans showed that the drag at those speeds was mainly turbulent, comparisonsbetween rigid bodies and cetaceans lead to uncertainties about the mix of laminar andturbulent flow, and, as a result of this uncertainty, frictional drag is unknown. This alsoleads to uncertainty of the pressure drag because the separation of the boundary layer isunknown. Surface drag also needs to be considered in the drag calculations, but becausethe amount of time cetaceans spend at the water surface is negligible, this number is84generally ignored. Muscle efficiency is also an uncertainty since either the muscles workmuch more efficiently than proposed or the animals encounter mainly laminar flow aroundthe body.While Purves (1963) explained how laminar flow is predicted to occur over the body atlow swimming speeds, it is still not understood how cetaceans deal with the turbulent flowthat is expected to occur at higher swimming velocities. To determine at what velocity ananimal experiences turbulent flow, as opposed to laminar flow, a dimensionless number,the Reynolds number (calculated by multiplying body length of the animal by its velocityand dividing this product by the viscosity of water) has been developed (Alexander 1982,1983, Vogel 1988). While drag is directly proportional to speed at low Reynoldsnumbers, it is approximately proportional to the square of velocity at high Reynoldsnumbers (i.e. Stokes’ law). Webb (1975) reports that in stable conditions, water flow overstreamlined bodies becomes turbulent at Reynolds numbers greater than about 5x106.Theoretical calculations of energy expenditure based on drag in cetaceans have beenpresented and many theoretical models have been developed to calculate drag at differentswimming velocities in cetaceans (Parry 1949, Lang 1961, 1965, Au and Weihs 1980,Lockyer 1981a, 1981b, Blake 1983). However, much uncertainty still exists becausecetacean hydrodynamics are not well understood.To try to resolve some of these uncertainties, COT was estimated both theoretically andfrom direct measurements in killer whales, Orcinus orca. Information on swimmingvelocities and breathing rates, together with measurements of oxygen consumption andstandard metabolic rates conducted on captive killer whales (Chapter 1), can yield an85estimate of COT and realized metabolic rates. However, for estimates of drag on killerwhales, measurements of the body and its appendages are necessary. The body can thenbe modelled as a cylinder with four appendages, the two pectoral fins, a dorsal fin andflukes, to use in calculations for drag estimates at different swimming velocities.Empirical data on killer whale’s COT during travelling were collected to compare killerwhale energy expenditures during travelling to theoretical data based on hydrodynamicmodels.In general, swimming killer whales take three to five short dives of 10 to 35 sec induration followed by a longer dive which can range from 1 to 10 mm or more (Norris andPrescott 1961, Lenfant et al. 1968, Leatherwood et a!. 1982, Baird 1994). Adult malekiller whales have been observed to dive for up to 30 mm (Bain pers. comm.). Thisbreathing pattern lends itself to studying the animals by theodolite tracking. Thistechnique (see Davis ci a!. 1981 for a discussion of theodolite surveying methodology) hasbeen a useful method in determining general movement patterns of cetaceans and killerwhales in localized areas (Kruse 1991, Wuersig ci a!. 1991) as well as for determiningswimming velocities and respiration rates of the animals. It is also possible to trackwhales by boat and measure the animals’ locations using a loran C device each time theysurface. Tracking whales by this procedure has the advantage that the length of the trackcan be increased relative to a theodolite, being limited only by bad weather and darkness.86In this chapter realized metabolic rates of wild killer whales are estimated using twoapproaches:a) determining the cost of transport (COT) of different age and sex classes of wild killerwhales by measuring swimming speeds, respiration rates and diving depths, andb) computing theoretical drag values for different sized killer whales at differentswimming velocities, and estimating the power required to overcome it.METHODSEnergy required for costs of transport and realized metabolic rates were estimated bymeasuring swimming velocities and respiration rates of free-ranging killer whales.Oxygen consumption rates measured in captive killer whales at the respiration ratesdetermined in free-ranging animals were used to estimate how much energy the animals inthe wild require to swim (see Chapter 1). Drag was estimated from morphometric data ofdifferent age and sex classes of killer whales and the data were analyzed for drag usingalready existing equations (Hoerner 1965, Blake 1983).Costs of transport, drag, and Reynolds numbers were calculated to determine the mostefficient swimming velocity. Tracks were only recorded when the whales were travelling.Travelling was operationally defined as members of the pod swimming in the samedirection (on the same course) at approximately the same swimming velocity, and nointeractive behaviour or feeding was observed (Ford 1994).87Swimming Sneeds. Respiration Rates and Diving Depthsa) Theodolite Study:The summer study area for free-ranging southern resident killer whales was easternHaro Strait on the west side of San Juan Island, Washington, USA. Between July andSeptember 1986 and May and September 1987 killer whales were observed at a siteapproximately 2 nautical miles south of the Limekiln Lighthouse (48° 30’N, 123° 1O’W).Data were collected between sunrise and sunset from a vantage point 74.5 m above meanlow low water (MLLW). This site provided an expansive view over Haro Strait as far asVictoria, ranging from South Bank (48° 29’N, 123°05’W) south of the observation site toBay (48° 30’N, 123° 29W) north of the site. Tracked whales travelled along the west sideof San Juan Island and were usually within 2 km of the coastline. The animals wereeasily observed and identified at a distance of 2 km and distinctive individuals up to adistance of 4 km. When a pod of whales was sighted, an individual animal which waseither in the lead, on the periphery, or at the rear of the group, was chosen as a focalanimal to avoid confusion with others. Individual killer whales were identified by saddlepatches and nicks and scratches on their dorsal fins and saddle patch area (Sugarman andShepard 1984, Bigg et al. 1987). Identification of an individual killer whale wasestablished by two observers.The theodolite was used to establish the vertical angle between the observation site andthe whal&s position during an exhalation. For each subsequent surfacing and respiration,new vertical angles and the horizontal angles between surfacings were measured(Figure 22).88—-77\ 4 I,,,//1 /2/\ I /Figure 22. Theodolite tracking of killer whales.89Observations of killer whales and measurements of diving distances were made using aSokkisha Electronic Digital Theodolite DT 20E, with a 160 mm telescope length and amagnification of 30x. The accuracy was within 20 s of arc. Individual animals and theirbehaviours were observed through the 30x spotting scope of the theodolite by the principalinvestigator and with 8x40 Leitz binoculars by an assistant.One observer (with binoculars) called out each time the whale came to the surface,while the other observer measured the whale’s position at each surfacing and recorded itwith a Sony portable tape recorder. This procedure was continued until the whaledisappeared from view or could no longer be positively identified.Several criteria were established to avoid incorrect measurements. Observations wererejected if any of the following occurred:1. there was any uncertainty about the whale’s identity during sampling,2. breaking waves were such that they could be mistaken for a spout (i.e., whale at thesurface),3. behaviours such as play, chasing fish or feeding took place, or4. the individual whale suddenly changed direction and/or changed position within thepod.During dives it was assumed that the whale swam in a straight line between surfacingpoints. After each observation session, the recorded data were transcribed onto datasheets, along with tide and current conditions at that time.90b) Southern and Northern Boat Studies:During the summer of 1988, observations of swimming killer whales and theirrespiration rates were made from a 6.2 m Thunderbird Cathedral Hull open boat. Theobservation area ranged from Iceberg Point on Lopez Island (48° 24’N, 122° 58W) toPoint Roberts (48° 55’W, 123° 00’W).From late April to mid June 1989, data were collected using the northern resident killerwhale population at the central coast of British Columbia. The area in which the animalswere observed ranged from Addenbrook Island (51° 36’N, 127° 53W) to Bella Bella (52°10’N, 128° 06’W), and NE as far as Nascall Island in Dean Channel (52° 40’N, 127° 15’W)and SE as far as South Bentinck Arm (51° 15N, 126° 56’W).While the driver of the boat and one other observer called out surfacings andrespirations, a third researcher noted the longitudes and latitudes at a distance ofapproximately 100 m from the focal whale using the loran. Locations of whales whenthey surfaced to breathe were made with a Micrologic ML-8000 loran C. The same fourcriteria mentioned above for minimizing invalid measurements were also applied to datacollection here.Diving depths were recorded after the loran tracking was finished and whenever it waspossible to have the whale swim under the boat. This sometimes required the boatoperator to move in front of the whale and to wait for the animal to swim beneath theboat. A Humminbird 400 D depth sounder was used to determine the depths at whichindividual whales swam below the boat. The driver of the boat navigated directly above adiving whale so that the animal was visible on the depth sounde?s screen. Due to the91large size of killer whales, it was unlikely to confuse whales with fish or other objects.To ensure correct identification of the focal animal while measuring diving depths, ananimal was chosen only if it was swimming by itself and at a distance of at least 200 mfrom any other whale.Analysisa) Track Distance CalculationsTo determine the distance the animals travelled between respirations, several variablesneed to be known: the height of the theodolite station and the vertical and horizontalangles of the location where the focal animal surfaced to breathe. The height of thetheodolite above the sea surface was determined with a Topgon GTS-3B infrared laserelectronic distance measurement total station theodolite and was corrected for tides frompredictive tide tables (Tide Tables, U.S. Dept. of Commerce, NOAA, 1986 and 1987).The distance between the theodolite station and the whale was calculated using the exactheight of the theodolite and the vertical angles measured by the theodolite. After thevertical angles were converted from degrees, minutes and seconds to fractions of degrees,the tangents of these angles were multiplied by the height of the theodolite to determinethe distance of the animal tracked from the theodolite. The horizontal angle measuredbetween two vertical angles determined the distance the animal had swum between tworespirations (see Figure 22). Again, minutes and seconds of the angle were converted tofractions of degrees, and the cosine of the horizontal angle was computed to determine thedistance between the two vertical angles to calculate the distance of two surfacings to the92shore. The successive positions were added to determine the distance over which theanimal was tracked along the water surface.Another spreadsheet was developed to convert the longitudinal and latitudinal data andobservation times into swimming distances and velocities. Differences between twoconsecutive latitudes and longitudes were determined. Longitudinal differences in minutesbetween the whale’s surfacing were multiplied by 1852, the number of meters in a nauticalmile. Longitudinal differences in minutes between surfacings were multiplied by 1150,the number of meters in a minute of longitude at the latitude where the observations wererecorded. The Pythagorean theorem was applied to calculate distances swum betweenrespirations. As with the theodolite data, the successive positions were added to calculatethe distance the animals had swum along the water surface.b) Dive ModelsEight theoretical dive models were developed to correct for distance travelled vertically(Figure 23). Models 1 to 4 did not have a fixed dive angle but suggested that the whalesdive to a determined depth, while models 5 to 8 have a fixed or no angle for descent andascent. Each whale track was tested with each dive model to determine which modelproduced the least variance in swimming velocity. A mean and variance was calculatedfor swimming velocity and measured between each surfacing. Variances produced by thedifferent dive models were compared and the dive model producing the least variance wasidentified as the best fitting model.93Dive ModelsDive Model Name Drawing Formula(Female) (Male)Box D+2*18 D+2*252*i()2+182 2*g()2+5V-Shape 2 21/3+2*I(ç)2÷182 +2*g(ç)2÷251/4÷2*.I()2÷182 ÷2*I()2÷2520 D D30 D+2*(2_)*18 D+2*(2_)*2545 D+2*(_1)*18 D+2*(_1)*2560D+2*Where D = surface distance measured by theodolite or loran in meters(18 and 25 represent estimated dive depths in meters for females and males, respectively)Figure 23. Potential dive profiles.94c) Swimming VelocitiesSwimming velocity, using the dive model which fit best, was determined from theequation:[19] Velocity = (Distance from the V-shaped model)/Time,where: Velocity = m/sec; Distance = meters; and Time = the total time elapsed (s) duringthe observation.The number of respirations the animal took were counted from beginning to end of eachtrack. Theodolite tracks were analyzed for bias in respiration rates due to time constraintsduring theodolite tracking. A regression equation of breathing rates as a function ofswimming velocities was calculated. Regression lines were then calculated between theresiduals and sample size both in duration of the track and in number of breaths. If theslope of the line is different than zero, it indicates the breathing rate is a biased estimateof metabolic rate.Observations were separated into mean swimming velocities and mean breathing ratesfor each age and sex category during summer and spring.Breathing rates were graphed as a function of swimming velocities for the different ageand sex classes for the different seasons.To determine whether it was appropriate to pool data of theodolite and loran tracks, ttests were used to compare slopes and intercepts of the regression lines for breathing ratesas a function of swimming velocity between seasons (Zar 1984). Respiratory intervals95were determined for each age and sex class for summer and spring seasons by comparingdive durations in summer and spring with a t-test.d) Cost of TransportCost of transport (COT) was approximated for each age and sex class of swimmingkiller whales using the following equation (Schmidt-Nielsen 1972, Tucker 1975, Sumich1983):[201 COTb [RR * (l000m/km) / (60/mm)] / velocity,where: COTb = breaths/km; KR respiration rate in breaths/minute; andvelocity = swimming speed in rn/sec.Metabolic rates were estimated by combining respiration rates measured in wild killerwhales with oxygen consumption per breath determined in captive killer whales (seeChapter 1). To correct swimming velocities for the correct activity state, the followingspeeds were assumed to fit the different activity states:a. 0 rn/sec to 0.5 rn/sec Activity state 1;b. 0.51 rn/sec to 2.0 rn/sec = Activity state 2;c. 2.1 rn/sec to maximum velocity measured = Activity state 3.For males, a mean oxygen extraction was calculated between Activity states 1 and 3 tocorrect for the missing Activity state 2. Oxygen consumption was then transformed intokcal/breath (see methods Chapter 1) and into kcal/kg/d, using mean body weights96calculated by Bigg and Wolman (1975) for the wild orcas: 5,000 kg for males(731.5 cm long), 2,800 kg for females (584 cm long), and 618 kg for the youngjuveniles (325 cm long).Metabolic rates were determined using respiration rates from wild killer whales basedon activity budgets (Ford 1984, Osborne 1986, Nichol 1990), and oxygen consumptionaccording to activity states from Chapter 1. The following equation was used:[211 MR = # of breaths taken/day * (kcal/breath) / M,where MR = metabolic rate (kcal/kg/day) and M is body mass in kg.Individual data points were entered into the Nonlin function in Systat and the best fittingequation was determined using the form:[22] MR. = a * Ve125,where MR = metabolic rate (kcal/kg/day); a = a constant; and Vel = swimming velocity inrn/sec.Metabolic rate was converted to COT using the following conversion:[23] COTC = (metabolic rate / velocity) * (l000rn / km )* (iday / 86400 s),where COTe = measured in kcal/kg/km; MR = kcal/kg/s (determined as in equation [21];and velocity = m/sec.97A curve was fitted rather than a straight line because the power required to overcomedrag increases with swimming velocity to the power of 2.5 to 2.8, depending on whetherthe flows are laminar or turbulent (Blake 1983).Morphometricsa) Fineness RatioMorphometric measurements of stranded or collected animals provided by Dale Riceand Al Wolman (National Marine Mammal Laboratory, Seattle, WA) were used tocalculate the fineness ratio of individual animals and assess streamlining; consequently,the coefficient of frictional drag is estimated from the fineness ratio for determining thedrag the animal is experiencing (Hoerner 1965). The fineness ratio was calculatedfollowing Webb (1975) and Feldkamp (1987):[24] FR = body length/maximum body diameter,where: FR is a dimensionless number and body length and diameter are measured in cm.b) Reynolds NumberReynolds numbers were calculated for differently sized animals swimming at differentswimming velocities (Blake 1983, Alexander 1983, Vogel 1988) to predict turbulenceeffects. The following equation was used:98[25] Re = LU/v,where: Re is a dimensionless number, L = body length (m); U = swimming velocity(rn/see); and v = the kinematic viscosity of water in m2/s.c) DragDrag was estimated following Blake (1983). The power needed to overcome drag isestimated as:[26] l/2p SwU3(kCD),where p = the viscosity of sea water; S,= the wetted surface area of the animal in m2;U = the velocity at which the animal is swimming in m/s; k = the excess drag due tochanges in body shape during swimming motions (dimensionless); CD = the coefficient ofdrag (dimensionless); and ö = the excess drag due to swimming near the surface(dimensionless).The kinematic viscosity of sea water at 10°C is 1.30777*106 m2 sec1 (Dorsey 1940).Morphometric data on stranded animals were used to estimate the wetted surface area ofthe animal. The area of the cylindrical body was calculated as length * girth. The area ofthe dorsal fin was calculated as two triangles (base * height), and the area of the flukeswas calculated as the span of the flukes * the width of the flukes. The surface area of thepectoral fins were calculated as the length of the fin * the width of the fin * 2. K islikely to have a value in the range of 1 to 4 (Blake 1983). ö was ignored because the99whales were assumed to spend a negligible time near the surface, and CD for an animalwith a fineness ratio of 5 is about 1.2 times Cf, which is the coefficient of frictional drag(Hoerner 1965). Cf scales with Reynolds numbe(°5 for laminar flow, and with Reynoldsnumber°2 for turbulent drag (Blake 1983). Metabolic rates at different swimming speedswere compared to the power needed to overcome drag.The proportion of laminar and turbulent flow was estimated as follows:1. the COT curve was fitted to the metabolic rate as a function of velocity data.2. drag was calculated for 100% laminar or 100% turbulent flow and the best fit of partiallaminar and turbulent flow was determined.The modelled COT based on estimated drag, postural cost, muscle efficiency and dragaugmentation factor was predicted as:Dp ÷ p ÷.smr .grn.r[271 COTdrag model = (1 t) ( CZTII.L ) ÷ ( CH1I.L )where: COTag model = kcal/kg/km, t = the fraction of turbulent flow, 1-t = the fraction oflaminar flow, smr = “postural cost” specific metabolic rate (kcal/kg/sec), which is theenergy required for swimming at a velocity of 0 m/s, D1 = the power to overcome dragdue to laminar flow (J/sec), D = the power to overcome drag due to turbulent flow(J/sec), c = the conversion from 3 to kcal (4.1873 = lkcal, Perez et a!. 1990) , m = massin kg, p = the efficiency of conversion of metabolic to movement energy, and v =swimming velocity in rn/s.100RESULTSObservationsOf a total of 157 observations of both theodolite and loran tracking, 82 were consideredacceptable. This constituted a total time of 42.27 hours and covered 238.23 km oftracking.Diving Depths and Dive ModelsThe mean diving depths measured with the depth sounder were 25 m for males, and 18m for females and juveniles. (Males: 5 = 25 m, n = 6, range = 21 to 27 m, SE = 0.93;females: i = 18 m, n = 4, range = 15 to 20 m, SE = 1.18; juveniles: 5E = 18, n = 3,range = 18 to 19 m, SE = 0.33).The model which fit the measured data most consistently for the measured distance overwhich the whales were tracked was the V-shaped model, described as:[28] 2* ,j[(Distance2/2)+depth2],where: Distance is in m and depth is in m.The seven models were compared for the 82 valid tracks. The V-shaped modelproduced the least variance in 64 (78%) of the 82 tracks and was used in further analysisto calculate the distance the whales travelled between surfacings.101BiasA bias towards overestimation of respiration rates existed for short theodolite tracks(Figure 24) as indicated by the negative slope of the regression lines. To eliminate this,all tracks less than 10 mm in length were shown in Figure 25 but not used for furthercalculations because it was believed that they did not accurately reflect respiration rates.In addition, because tracks started and ended with surfacings which did not always pickup an integral number of respiratory cycles, too many surfacings were measured over thedistance travelled in some cases. To correct for this overestimation of respirations, theinitial breaths and corresponding times were eliminated so that all tracks began with along respiratory interval and ended with a breath, except for tracks where respiratoryintervals were uniform. This method reduced the bias, and the bias was negligible after10 mm of theodolite tracking. Respiration rates as a function of swimming velocity forjuveniles were graphed (Figure 25c). Because metabolic rates determined fromrespiration studies (see Chapter 1) were not available, further analysis of data fromjuveniles was precluded.Breathing Rates and Swimming VelocitiesSimple linear regressions were fitted to the data of breathing rates of adult males, adultfemales and juveniles during summer and spring as a function of swimming velocities(Figure 25, Table 20 and 21). Data for males in summer and spring were pooled afterdetermining that the slopes and intercepts of the individual seasonal regression lines didnot differ statistically (slopes: t=0.46, p>O.5; intercepts: t=0.89, p>0.2). The pooled102U) a) N — CØ) a) II120 100 80 60 40 20 0C-1-0.500.51Bias(Observed-ExpectedBreaths /Mm)1.5[-breathstimeFigure24.Relationofbiasinbreathingratetosamplesizeforfemales.(a)8Swimming Velocity (mis)— 61*32&.d.dI 0 i.*d.0<18 =(b) 43.51 . ... ... .2.5 - 0...... - _...08Swimming Velocity (m/s).âIoo— —,924ddR) th1O(c)3.5 ..3 ..v2.5 90Swimming Velocity (m/s)a•od.anlo., a — l.2+I9l(p,,l.d&) 0 thodo0.<10Figure 25. Respiration rates as a function of swinnningvelocity in killer whales.(a) males, (b) females, (c) calves and juveniles.104Table20.Swimmingvelocitiesandbreathingratesinfree-rangingkillerwhalesduringthesummerandspring.SummerISpringStandardNumberofIStandardNumberofMeanVelocity(mis)MeanRangeDeviationObservationsMeanRangeDeviationObservationsmales2.410.9-4.71.1622I2.470.9-3.60.9815females2.401.5-4.40.8116I2.390.9-4.11.0616juveniles2.160.5-4.40.9615I2.060.8-3.20.918MeanBreathingRateI(breaths/mm)males1.580.9-3.40.58221.330.5-2.50.4715females1.721.4-2.10.2816I1.330.7-1.80.3816juveniles1.791.2-2.70.4315I1.280.6-1.70.488Table 21. Regression equations and statistics for the relationship between respiration rates(PR in breaths/mm) and swimming velocities (mis) in male, female and juvenile killer whales.Sex Equation Number of r2 Significance SE of y SE of xObservations Level Intercept CoefficientMales RR = 0.61 + 0.32Vel 37 0.41 p <0.001 0.42 0.06Females RR=0.92+0.24Vel 32 0.36 p<O.OO1 0.30 0.06Juveniles RR= 1.19+0.2OVel 23 0.14 p<O.1 0.47 0.11106regression analysis for adult males showed a significant correlation between breathing rateand velocity (r20.41, N=37, df=35, p<O.OO1). For adult females, the summer and springdata were pooled as well; while the slopes were not statistically different from each other,the intercepts were significantly different (slope: t=1.66, p>O.l; intercept: t=3.77,p<O.OOl). Although the summer data were corrected for bias, the differences may be dueto sampling technique. Despite the differences, data were pooled and the pooled regressionline showed significant correlation (r2=0.36, N=32, df=30, p < 0.001). While the slopes ofthe regression lines between respiration rates and swimming velocities for males andfemales did not differ (df = 2, df = 88, F = 0.74, p > 0.5), the intercepts were significantlydifferent (df = 9, df = 90, F = 134.5, p < 0.001). Interseasonal comparisons betweenjuveniles are significantly different from each other.Metabolic RatesMetabolic rates during travel at different swimming velocities for males (Figure 26a)were calculated as:[29] MR (kcal/kg/d) = 29.317 + 1.109 V25,where V is the swimming velocity in rn/sec.For females (Figure 26a), this equates to:[30] MR (kcallkg/d) 32.285 + 1.256 V25.107(a) 1201002:Swimming Velocity (mis)(b) io100Swimming Velocity (mis)Figure 26. Metabolic rate as a function of swimming velocity in killerwhales. (a) males, (b) females.108While the slopes of the two regressions of log-transformed data were not statisticallydifferent (t = 0.67, df = 65, p > 0.5, the intercepts were significantly different (t = 15.7,df 66, p <0.00). No further calculations could be conducted with data from juvenilesbecause metabolic rates could not be determined by respiration analysis in captivity.Cost of TransportThe minimum COT at which the male killer whales took the least breaths/km was at ameasured velocity of 3.1 rn/s (Figure 27a) and corresponds to 0.18 kcal/kg/km. For adultfemales, the lowest COT was measured at 3.1 rn/s (Figure 27b) with an energetic outputof 0.2 kcal/kg/km.Mori,hometricsa) Fineness RatioFineness ratios were calculated for each individual animal for which data on length andgirth were available (Table 22). The values of fineness ratio ranged from 4.51 to 5.87,with a mean of 4.96. The position of the maximum diameter along the body wasestimated from 13 animals, and ranged from 30-43% behind the snout with a mean of36%. The surface areas of the different appendages are also presented (Table 22). Fromthese data, the surface area was calculated to be 23.07 m2 for an adult male killer whale at7.4 m and a calculated weight of 5153 kg (Bigg and Wolman 1975), 13.17 m2 for afemale measuring 5.79 m (2738 kg), and 3.86 m2 for a juvenile at an approximate age of2 years (3.19 m; 589 kg).109(a) 0.5Swimming Velocity (mis)(b) o.0.150.1 --0.050 1111111111 1111110 0.5 1 1.5 2 2.5 3 3.5 4 4.5Swimming Velocity (mis)Figure 27. Cost of transport of male (a) and female (b) killer whalesas a function of swimming velocity.110Table 22. Body measurements of stranded killer whales.Animal Sex Length Girth Base of Height of Span of Width of(m) (m) Dorsal Fin (m) Dorsal Fin (m) Flukes (m) Flukes (m)1965-4 M 7.4 4.88 1.18 1.3 2.3 0.61Namu M 6.56 3.85 0.9 1.2 2.05 0.471970-101 M 3.19 2.12 0.39 0.43 0.77 0.181972-3 M 2.99 2.07 0.43 0.34 0.76 0.251963-832 M 7.24 4.84 0.92 1.45 2.55 0.75US-60-1 M 5.18 2.77 0.56 0.63 1.38 0.39US-61-IK M 7.6 4.69 1.17 1.66 2.73 0.623204 M 6.3 3.9 0.9 0.98 2.1 0.53264 M 3.85 2.6 0.66 0.48 1.06 0.293266 M 6.98 4.52 1.17 1.37 2.36 0.621962-605 M 6.86 4.78 1.07 1.52 2.44 0.711964-986 F 5.65 3.44 0.68 0.6 1.48 0.43265 F 5.79 3.68 1.07 0.71 1.58 0.493774 F 4.92 2.93 0.72 0.63 1.38 0.36Lenght of Width of Weight Body Dorsal Fin Fluke Area Pectoral Fin TotalPect. Fins (m) Pect. Fins (m) (kg) Area (mZ) Area (m2) (mZ) Area (m2) Appendages (m2)1.33 0.78 5153 18.06 1.53 1.40 2.07 5.011.37 0.75 3778 12.63 1.08 0.96 2.06 4.100.39 0.22 589 3.38 0.17 0.14 0.17 0.480.43 0.23 499 3.09 0.15 0.19 0.20 0.531.6 1.04 4871 17.52 1.33 1.91 3.33 6.570.75 0.42 2055 7.17 0.35 0.54 0.63 1.522.05 1.22 5520 17.82 1.94 1.69 5.00 8.641.1 0.63 3404 12.29 0.88 1.05 1.39 3.320.61 0.3 957 5.01 0.32 0.31 0.37 0.991.6 0.9 4433 15.77 1.60 1.46 2.88 5.951.52 1.02 4239 16.40 1.63 1.73 3.10 6.460.79 0.41 2571 9.72 0.41 0.59 0.65 1.650.96 0.51 2738 10.65 0.76 0.77 0.98 2.510.74 0.35 1800 7.21 0.45 0.50 0.52 1.47Surface Log Log Surface Appendage Body Surface FinenessArea (m) Weight (kg) Area (ma) Volume (m’) Surface Volume (ni) Volume (n?) Ratio23.07 3.71 1.26 4.48 0.97 3.50 4.7616.73 3.58 1.10 4.43 1.08 3.34 5.353.86 2.77 0.53 6.55 0.81 5.74 4.733.63 2.70 0.49 7.28 1.07 6.21 4.5424.10 3.69 1.24 4.95 1.35 3.60 4.708.70 3.31 0.86 4.23 0.74 3.49 5.8726.46 3.74 1.25 4.79 1.56 3.23 5.0915.60 3.53 1.09 4.58 0.97 3.61 5.076.00 2.98 0.70 6.27 1.03 5.23 4.6521.72 3.65 1.20 4.90 1.34 3.56 4.8522.86 3.63 1.21 5.39 1.52 3.87 4.5111.37 3.41 0.99 4.42 0.64 3.78 5.1613.17 3.44 1.03 4.81 0.92 3.89 4.948.68 3.26 0.86 4.82 0.82 4.00 5.28111b) Reynolds NumberReynolds numbers ranged for males from 5* 106 at a swimming speed of 0.43 m/sec to5*107 at 4.76 rn/sec. For females, Reynolds numbers ranged from 3.9*106 at 0.88 m/secto 1.9*107 at 4.39 rn/sec, and for juveniles, the range was from 1*106 at 0.45 rn/sec to1*107 at 4.39 rn/sec.c) DragAssuming that 30% of the energy consumed by muscles is used to overcome drag[which lies within the range of general assumptions and Blake (1983) assumed 25% fordolphins], and k=2 (the excess drag due to changes in body shape), then 88% of the flowwas laminar, and 12% turbulent for males (Figure 28a). For females, 89% of the flowwas laminar and 11% turbulent using the same assumptions (Figure 28b).DISCUSSIONDive ModelsThe V-shaped dive model provided the best fit in 78% of all tracks tested and wastherefore used to complete distance calculations for all tracks. Similar dive types in killerwhales were recognized by Baird (1994) using a recoverable, suction-cup attached timedepth recorder (TDR) VHF radio-tag. Baird (1994) reported that the proportion of thedifferent dive types varied with dive duration, dive depths and behaviour of the animals,but that the majority of the whales’ time was spent at depths less than 20 m from the112‘-..-i.....-..-.---.....----.-.---.-—.---.--.—-.----..‘‘‘—\..-.-..-.-—.*.._-.....‘.....::.-..,. .=....:..:.::.:........-....I I I I I I I—. Iin WthuI,t fittdcfrg(88-12)[jmis In twoIt d&(89-11)Figure 28. Comparison of COT based on respiration asa function of swimming velocity and fitted dragmodels for killer whales. (a) males, (b) females.(a) 0.30.2____________0.100 1 2 3 4 5Swimming Velocity (m / s)(b) 10.90.8‘-‘0.7L.60.5CC>—.-1...._...._... .. —.——...... .-.—.I I I I I I I1 2 3 4Swimming Velocity (m / s)0 5113surface. The small number of measured diving depths in my study on travelling killerwhales suggests that killer whales do not dive to deep depths during travelling. Baird(1994) for killer whales, and Le Boeuf et at. (1993) for pinnipeds, suggested that longerdive durations and deeper diving depths may be associated with prey searching behaviour.Because swimming velocities and diving depths were only measured during travellingbehaviour, no deep diving depths were measured in this study as have been reported forkiller whales (Heezen and Johnson 1969, Bowers and Henderson 1972).Diving to deep depths during travelling would increase the total distance the animal hasswum during the time it was tracked. Determining diving profiles and direction anddetermining depths with recently developed sonar equipment will better determine divingdepths during travelling by cetaceans in future studies.BiasDue to a bias in respiration rates as a function of swimming velocities during shorttheodolite tracks, all tracks less than 10 mm in duration were discarded and all otherswere corrected to begin with a long dive interval. While difficulties and errors associatedwith incorrect measurements and inaccuracy in theodolite tracking have been reviewed(Wuersig et a?. 1991), the recognition of bias due to short tracks has not been previouslyreported. For future studies, it can be recommend using only tracks longer than 10 to 15mm in length to ensure a representative sample of breathing rates as a function ofswimming velocity.114Respiration Rates. Swimming Velocities and Metabolic RatesMeasured maximum swimming velocities were slower (7.4 m/s) than the reportedmaximum speeds measured in killer whales in the open sea over short distances of about15.4 m/s (Lang 1966).A linear relationship between respiration rates and swimming velocities was found forall age and sex classes of killer whales, while the relationship of metabolic rate as afunction of increasing swimming velocity was curvilinear. This suggests that respirationrates and metabolic rates are not related linearly to each other, hence by just collectingrespiration rates in marine mammals, energy demands cannot be deduced directly fromrespiration rates. Curvilinear relationships between metabolic rates and increases inswimming velocity have also been determined in other swimming animals, such as in fish(Brett 1964), turtles (Prange 1976), ducks (Prange and Schmidt-Nielsen 1970), mink(Williams 1983), sea otters (Williams and Kooyman 1985), and seals (Davies et a?. 1985).For terrestrial mammals and birds running on a treadmill, metabolic rate increases linearlywith speed (Taylor et a?. 1970, Taylor et a?. 1982, Schmidt-Nielsen 1990).Cost of TransportThe male and female killer whales in this study reached their lowest cost of transportbetween 0.18 kcallkg/km and 0.2 kcal/kg/km at a velocity of 3.1 rn/s. These results fit invery well with data reported in the literature: gray whales’ (Eschrichtius rob ustus),weighing 15 t, minimum cost of transport is 0.1 kcal/kg/km at 2.0 to 2.2 m/s (Sumich1983, 1986); bottlenose dolphins (Tursiops truncatus) weighing only 145 kg, reached a115minimum COT with 0.31 kcal/kg/km at 2.1 rn/sec (Williams et al. 1992). Comparing theenergy for COT in cetaceans to that of theoretical fish of similar sizes, cetaceans requiremore energy than fish. Male killer whales used 2.9 times the predicted value of energyexpenditure of a 5,000 kg fish, while females were very close to the value of males with2.8 times the predicted energy used by a fish of 3,000 kg (Brett 1964). Sumich (1983,1986) calculated gray whales’ COT as 2.6 times that of a fish of comparable size;bottlenose dolphins’ COT is 2.1 that predicted for a fish of the same size (Williams 1992).In harbour (Phocoena vitulina) and harp seals (Pagophilus groenlandicus) (Craig andPasche 1980, Lavigne et a!. 1982, Davis et al. 1985), the cost of transport was 3-4 timeshigher for yearling and adult animals than for salmon extrapolated to the same size as thepinnipeds. However, when comparing marine mammals’ COT to that of other aquatic andsemi-aquatic animals such as mink (Williams 1983), sea otters (Williams 1989) and ducks(Prange and Schmidt-Nielsen 1970), cetaceans and pinnipeds have considerably lowerCOT’s. Humans are extremely inefficient swimmers: their COT is 8-12 times thatpredicted for dolphins (Williams 1992). It is interesting to note that the averageswimming velocities observed during summer in killer whales in both the southern andnorthern residents (2 m/s) (this Chapter, Kruse 1991) is lower that their energeticallyoptimal swimming speed of 3 m/s, at which the animals’ COT is lowest. While thedifference in caloric expenditure of swimming between 2 and 3 rn/s is only 0.05kcal/kg/km for male and female killer whales, the slightly lower than optimal velocitymay be related to the behaviour in which the animals are engaged. During late spring andsummer, salmon swim in large schools through Haro and Johnstone Strait (Heimlich116Boran 1986, 1988, Nichol 1990) and northern and southern resident killer whales followthese salmon stocks (Felleman et al. 1988). Similar differences in swimming velocityhave been reported for seals (Thompson et al. 1993).Fineness Ratio. Reynolds Numbers and DragThe fineness ratio is representative of the quality of body streamlining, and, therefore,of the efficiency of streamlining in reducing drag among solid bodies (Williams andKooyman 1985). The values for the fineness ratio calculated for the killer whales forwhich morphometric data were available indicated that killer whales have fineness ratios(4.51 to 5.87 with a mean of 4.96) close to the optimum of 4.5, indicating a body shapewhich produces a minimum drag for a maximum body volume (Webb 1975, Feldkamp1987). In comparison, fineness ratios ranged from 3.8 to 5.5 for a variety of cetaceansand large fishes (Hertel 1966) and from 5.5 to 7.0 in fishes which swim in thesubcarangiform mode (Webb 1975).Reynolds numbers were calculated for all velocities. For velocities greater than 1 rn/sturbulent flow is predicted (Re > 5x106,Webb 1975) for males and females, whilejuveniles started to encounter turbulent flow at a swimming velocity of 1.4 rn/s.Drag in marine mammals is poorly understood and empirical data have only beencollected on carcasses (Williams and Kooyman 1985), and data have been approximatedtheoretically. Drag was estimated for adult male and female killer whales, however,several unknown variables had to be assumed as mentioned in the methods of this chapter.Drag estimates are based on three unknown and only assumed factors: k, the excess drag117due to changes in body shape during the swimming motion, which ranges between 1 and4 where it has been measured. Blake (1983) assumed k=4 for a hypothetical dolphincalculation. The efficiency of the muscle for marine mammals is unknown; Blakeassumed this to be on the order of 25%. Last, the amount of laminar and turbulent flowis not known; while the adult killer whales in this study had Reynolds numbers indicatingturbulent flow across the body, the Reynolds numbers for juveniles at swimming velocitiesless than 1.4 m/s were low enough to suggest laminar flow. Based on theoreticalcalculations, the adult males and females should encounter turbulent flow over themajority of their body area if swimming faster than 1 m/s. When the drag curve wasfitted to the COT curve for the different sex classes, however, this was not observed: themajority of flow was laminar (89% for males and 88% for females). While the maximumdiameter along the animaUs body is located 36% of the body length behind the rostrumand this position is far enough back to ensure laminar flow over the forward portion of theanimal and reduce drag (Hoerner 1958), the fitted laminar flow of 88% in males and 89%in females (Figure 28) is still 52% and 53% higher than expected for male and femalekiller whales respectively. In harbour seals, the drag coefficient was determined to be lessthan that found on humans, cars, submarines and torpedo shapes (Williams and Kooyman1985). This suggests that the water flow around the body of seals is relatively smoothwhich can also be observed when seals are seen swimming through bioluminescentplankton (Williams and Kooyman 1985). The same has been observed for Dall’sporpoises (pers. obs.) and dolphins (Stevens 1950, Hill 1950).118Estimated Daily Caloric ExpenditureEnergetic expenditures can be estimated by approximating daily behaviour budgets withactivity states studied in Chapter 1. On average, free-ranging killer whales spend 71% oftheir time travelling and foraging, 13% resting, and 15% socializing, including rubbing,during the summer months (Ford 1984, Osborne 1986, Nichol 1990, Ford et a!. 1994).The travel/forage behaviour was approximated with Activity states 2 to 3, rest and rubbingbehaviour with Activity state 1, and social behaviour was approximated with Activity state3. Using an intermediate value between Activity states 2 and 3 for the travel/foragecategory, the best estimate for caloric requirements is 184,900 kcal/d for adult males and136,500 kcal/d for adult females. Using these estimates, and approximating thetravel/forage mode with Activity state 2 or Activity state 3, the estimate for male killerwhales ranges from 150,700 kcal/d to 225,730 kcal/d, while female killer whales requirefrom 108,420 kcal/d to 164,400 kcal on a daily basis.119Chapter 4: SUMMARY AND CONCLUSIONSThis chapter summarizes the different components of the energy budget of killer whalesin captivity and in the wild and identifies research topics that require further considerationand experimentation. Energy utilization, including faeces, apparent digestible,metabolizable, maintenance and production energy, has been examined for many differentspecies of wild and domestic animals (Brody 1945, Harris 1966, Kleiber 1975). Forcetaceans, some of the components of the bioenergetic model have been examined(Lockyer 1981a, 1981b, Lavigne eta?. 1982, Innes et a?.1987), but to date it has not beenpossible to quantify all of the different components for a single cetacean species throughactual measurements. The problems of conducting experimental work with cetaceans havebeen raised in the previous chapters. Nevertheless an attempt to quantify the energybudget of the killer whale, Orcinus orca, has been made. It should be remembered that thevariables measured may be altered somewhat by the conditions of captivity but correctionsfor this were attempted where necessary. At the same time data collection directly fromkiller whales in the wild also posed considerable problems in obtaining a representativesample of the wild population. These problems are not unique to this study and havebeen discussed by others (Caughley 1966, Brodie 1975, Lockyer 1981a, 1981b, Lavigneet a?. 1982, Innes et a?. 1987).While variations exist and the problems pointed out should not be overlooked, theyshould not deter scientists from studying cetaceans and other marine mammals from amore holistic point of view than has been done in the past.120It has been suggested by many (Kanwisher and Sundnes 1965, Irving 1972, Slijper1979, Kasting et a!. 1989) that the standard metabolic rates of marine mammals andcetaceans, and killer whales in particular, are higher than those of terrestrial mammals.However, measurements of oxygen consumption by unrestrained captive male and femalekiller whales indicate the SMR is between 1.2 and 1.3 times that of Kleiber’s (1975)prediction of basal metabolic rates, hence comparable to terrestrial carnivores of the samesize (McNab 1982). Others (Oritsiand and Ronald 1975, Gallivan 1977, Parson 1977)have found that basal metabolism in confined pinnipeds is near, and even below, Kleibe?s(1975) equation for mammals.While the killer whale& tidal volumes at rest are between 2.65 and 4.18 times higherthan those of terrestrial mammals, the vital capacities of these animals are between 68 and94% that of terrestrial mammals of comparable size (Stahl 1967) and fall within valuessuggested for cetaceans (Dolphin 1987). Oxygen measurements at different activity ratesshowed that killer whales take up 02 at higher rates at higher activities; the minimumestimate of metabolic scope of orcas of about 6 is between 30 and 50% smaller than thatobserved in most terrestrial mammals. However, these metabolic scopes are most likelyunderestimated because the whales were not pushed to their maximum limits of exertion.The quantity of food ingested per meal, the frequency of feeding, the amount ofdifferent food items consumed and the caloric equivalents of these food items can beobtained from food records for captive animals. While food items of wild killer whales arewell known and have been reviewed (Rice 1968, Castello 1977, Slijper 1979, Heyning1988, Thomas and Felleman 1988, Wenzel and Sears 1988, Hoyt 1990), the amounts of121food consumed by wild animals have not been determined. As expected, husbandryrecords from captive orcas indicate that food intake increases with increasing body mass,but decreases on a per body weight scale (Food Intake = 0.277 M°663, whereM = body mass in kg).More information about the regulation of food intake from the animal’s point of view isgained from examining seasonal variation in food intake together with effects of watertemperature. Very little or no (<1.3% / °C) variation was found for captive killer whales,suggesting that normal activity produces sufficient heat to maintain body temperature inwater ranging from 70 to 23°C.During the female killer whales’ approximately 17 months of gestation (Walker et a!.1988), food consumption varied < 25% from food intake prior to pregnancy, whereas theenergetic cost during lactation was twice that of previous non-pregnant levels. Whilepregnancy is not expensive energetically, lactation is very costly.By comparing the food consumed to the energy expended determined by respirationanalysis, the mean net assimilation efficiency (NAE) of captive killer whales wascalculated to be 0.73, a high food utilization compared to terrestrial mammals but similarto NAE’s reported for other marine mammals [0.67- 0.97 (Shapunov 1972a, 1972b,Lavigne et a!. 1981, Yasui and Gaskin 1986, Worthy 1990)1.The diurnal activity patterns of killer whales are well documented in captivity (Bain1986, Ray et al. 1986) and also in the wild during day time activities (Ford 1984, Osborne1986, Nichol 1990). By assigning caloric expenditures to the different activities andsumming those over a 24 h period, estimated caloric expenditures indicate that killer122whales’ energetic necessities closely fit findings for other cetaceans (Innes et a!. 1987) aswell as those for terrestrial mammals of similar size.By studying free-ranging killer whales to estimate energetic expenditures duringswimming, observations longer than 10 mm and preferably 15 mm in duration werenecessary to obtain unbiased theodolite data on respiration rates as a function ofswimming velocity. While the relationship of respiration rates as a function of swimmingspeed was linear for all age and sex classes, they were different for each gender and agecategory. Metabolic rates and cost of transport (COT) as functions of swimming velocityas well as the optimal COT were shown to be curvilinear in shape as found for otheraquatic animals. Maximum range velocities occured at a velocity of 3 m/s for adult malesand females. To swim efficiently and to reduce drag, it was shown that killer whales havean almost ideal fineness ratio of 4.51 to 5.87 (mean = 4.96). Drag was higher thanpredicted for a rigid body but lower than expected for a flexible body. Flow wasinterpreted to be much higher in laminar content than expected from theoreticalassumptions reported in the literature. Values were inferred for a number of parametersthat still need to be determined individually. Certain adaptations such as streamlining anda fusiform body shape as well as the reduction of hair on the body surface aid inincreasing laminar flow occurring over the body. However, more adaptations, which atthis point are not understood, are necessary to swim as efficiently as cetaceans and othermarine mammals do.Captive studies together with observations of wild animals can yield valuableinformation on how much energy animals must expend for standard metabolic rates and123daily activities. They also provide insights into how efficiently an animal uses the energyit has available for locomotion. Estimating realized metabolic rates from the activities offree-ranging killer whales, combined with oxygen consumption information from captiveorcas, showed that realized metabolic rates of wild killer whales are 25-33% higher thanestimates for the two captive adult animals. This discrepancy might be accounted for bythe differences in activity levels and reproductive status between captive and wild animals.Much more research, using new technologies for wild whales and trained whales incaptivity, can be conducted to increase the knowledge we have at this time. Laminar flowaround a cetaceans’ body can be determined with animals in captivity, using recentlydeveloped equipment. By visualizing water flow around a killer whale’s body, thecalculated estimate of the proportion of laminar and turbulent flow could be verified.More data during very slow (<1.5 m/s) and fast (>4 m/s) swimming should be collectedto determine whether some of the data points occuring at low and high swimmingvelocites as seen in the COT curves of male and female killer whales possibly correspondto the different gaits as seen in moving horses (Schmidt-Nielsen 1990). Respirationcollections could be obtained from trained juvenile killer whales in other aquaria.Combining those respiration data with respiration rates correlated with different swimmingvelocities measured in wild juvenile animals, COT’s can be determined for all age classesof killer whales. Following this, the sharing of the cost of locomotion, by which femalekiller whales assist young whales in locomotion by swimming in the echelon position(Waite 1988), can be quantified energetically and hydrodynamically. Fadely et a!. (1990)developed a new technique to determine net assimilation efficiencies from the collection124of partial fecal samples. Samples of killer whale feces can be collected in aquaria toanalyze for NAE and to compare those findings to the calculated NAB determined here.By knowing the quantity of food required by different age and sex classes of killerwhales, and by knowing how many killer whales frequent areas of valuable fish sources,such as with the blackcod (AnoplopomajImbria) industry in Alaska (Matkin 1988) anddifferent salmon species (Oncorhynchus sp.) in British Columbia and Washington waters,the impact of depredation on these fish species by killer whales can be estimated.While it is extremely difficult, if not currently impossible to conduct many aspects ofphysiological and behavioural studies on wild cetaceans, imaginative ways of combiningstudies of captive cetaceans with research conducted on free-ranging whales and dolphinscan help shed light on some aspects of the life of marine mammals. Many moreintriguing questions about cetaceans are unsolved. While it is not possible to answer allof these questions, undoubtedly many more will be solved with improving technology andnew ways of thinking about scientific research.125LITERATURE CITEDAlexander, R.M. 1982. Locomotion of animals. Blackie, London.Alexander, R.M. 1983. Animal mechanics. Blackwell Scientific Publications, London.Andersen, S. 1965.Ltalimentation du marsouin (Phocoenaphocoena) en captivite. VieMilieu 12:799-810.Asper, E.D., W.G. Young and M.T. Walsh. 1988. Observations on the birth anddevelopment of a captive born killer whale. mt. Zoo Yearbook 27:295-304.Association of Organic and Agricultural Chemists 1984. Official methods of analysis. 14thEdition, Arlington, Ohio, USA.Armstrong, A.J. and W.R. Siegfried. 1991. Consumption of Antarctic krill by Minkewhales. Antarctic Science 3:13-18.Au, D. and D. Weihs 1980. At high speeds dolphins save energy by leaping. Nature284:548-550.Bain, D.E. 1986. Acoustic behaviour of Orcinus: periodicity, behavioural correlates andan automated technique for call classification. Pp. 335-372, in. Kirkevold, B.C. andJ.S. Lockard (eds.), Behavioural biology of killer whales. Alan R. Liss, New York.Bain, D.E. 1990. Examining the validity of inferences drawn from photo-identificationdata, with special reference to studies of the killer whale (Orcinus orca) in BritishColumbia. Rep. Tnt. Whal. Comm. 12:93-100.Baird, R.W. 1994. Foraging behaviour and ecology of transient killer whales (Orcinusorca). Ph.D. Thesis. Simon Fraser University, Burnaby, B.C. 157 pp.Beach, R.J., A. C. Geiger, S.J. Jefferies, S.D. Treacy, and B.L. Troutman. 1985. Marinemammals and their interactions with fisheries of the Columbia River and adjacentwaters, 1980-1982. Third Annual Rep. NOAA, NMFS.Benedict, F.G. 1938. Vital Energetics: a study in comparative basal metabolism. Carnegie,Institute. Washington, D.C.Bigg, M.A., P.F. Olesiuk, and G.M. Ellis. 1990. Social organization and genealogy ofresident killer whales (Orcinus orca) in the coastal waters of British Columbia andWashington State. Rep. Tnt. Whal. Comm. 12:383-405.126Bigg, M.A., G.M. Ellis, J.K.B. Ford and K.C. Balcomb. 1987. Killer Whales. PhantomPress, Nanaimo, B.C.Bigg, M.A. 1982. An assessment of killer whale (Orcinus orca) stocks off VancouverIsland, B.C. Rep. Intl. Whal. Commn 32:655-666.Bigg, M.A. and A.A. Wolman. 1975. Live-capture killer whale (Orcinus orca) fishery,British Columbia and Washington waters, 1962-73. J. Fisheries Res. Board Can.,32: 123 1-122 1.Blake, R.W. 1983. Energetics of leaping in dolphins and other aquatic animals. J. Mar.Biol. Assoc. U.K. 63:61-70.Blaxter, K. 1989. Energy metabolism in animals and man. Cambridge University Press,Cambridge, MA.Bowers, C.A. and R.S. Henderson. 1972. Project Deep ops: deep object recovery withpilot and killer whales. Naval Undersea Center Technical Paper No. 306, SanDiego, CA.Brett, J.R. 1964. The respiratory metabolism and swimming performance of youngsockeye salmon. J. Fisheries Res. Board Can 21:1183-1226.Brodie, P.F. 1975. Cetacean energetics, an overview of intraspecific size variation.Ecology 56:152-161.Brody, S. 1945. Bioenergetics and growth. Reinhold, Baltimore, MA.Bryden, MM. 1988. Adaptations to the aquatic environment. Pp. 110-121, in: Harrison,R., and Bryden, M.M. (eds.) Whales, dolphins and porpoises. Facts on File, NewYork, N.Y.Castello, H.P. 1977. Food of a killer whale: eagle sting-ray, Myliobatis found in thestomach a stranded Orcinus orca. Sci. Rep. Whales Fres. Inst. 29:107-111.Caughley, G. 1966. Mortality patterns in mammals. Ecology 47: 906-9 18.Costa, D.P. 1987. Isotopic methods for quantifying material and energy intake in freeranging marine mammals. Pp. 43-66, in. AC. Huntley, D.P. Costa, G.A.J. Worthy andMA. Castellini (eds.), Marine mammal energetics. Allen Press, Lawrence, KS.127Craig, A.B. and A. Pasche. 1980. Respiratory physiology of freely diving harbor seals(Phoca vitulina). Physiol. Zool. 53 :419-432.Davis, R.E., F.S. Foote, J. Anderson and E. Mikhail. 1981. Surveying theory and practice.6th. Edition, McGraw Hill, New York.Davis, R.W., T.M. Williams, and G.L. Kooyman. 1985. Swimming metabolism of yearlingand adult harbor seals Phoca vitulina. Physiol. Zool. 58:590-596.Dolphin, W.F. 1987. Dive behavior and estimated energy expenditure of foraginghumpback whales in southeast Alaska. Can. J. Zool. 65:354-362.Dorsey, N.S. 1940. Properties of water substance. American Chemist Society, RheinholdPubl. Services, New York.Duffield, D.A. and K.W. Miller. 1988. Demographic features of killer whales in oceanariain the United States and Canada, 1965-1987. Pp. 297-306, in: J. Sigurjonsson and S.Leatherwood (eds.), North Atlantic killer whales. Pit Fiskideildar, Vol. 11, Reykjavik.Fadely, B.F., G.A.J. Worthy, and D.P. Costa. 1990. Assimilation efficiency of northernfurs seals determined using dietary manganese. J. Wildi. Manage. 54:246.Feldkamp, S.D. 1987. Swimming in the California sea lion: morphometrics, drag andenergetics. J. Exp. Biol. 13 1:117-135.Felleman, F.L., J,R. Heimlich-Boran, and R.W. Osborne. 1991. The feeding ecology ofkiller whales (Orcinus orca) in the Pacific Northwest. Pp. 79-112, in: K. Pryor andK.S. Norris (eds.), Dolphin societies. University of California Press, Berkeley, CA.Ford, J.K.B. 1984. Call traditions and dialects of killer whales (Orcinus orca) in BritishColumbia. Ph.D. Thesis, University ofBritish Columbia, B.C.Ford, J.K.B., G.M. Ellis and K.C. Balcomb. 1994. Killer whales. UBC Press, Vancouver,B.C.Evans, P.G. 1987. The natural history of whales and dolphins. Facts on File, New York,N.Y.Gallivan, G.J. 1977. Temperature regulation and respiration in the freely diving harp seal(Phoca groenlandica). M.Sc. Thesis, University of Guelph, Guelph, Ontario.Gaskin, D.E. 1982. The ecology of whales and dolphins. Heinemann, London and Exeter,N.H.128Gray, J. 1936. Studies in animal locomotion, J. Exp. Biol. 13:192-199.Hampton, I.F.G. and G.C. Whittow. 1976. Body temperature and heat transfer in theHawaiian spinner dolphin, Stenella longirostris. Comp. Biochem. Physiol. 55A: 195.Harris, L.E. 1966. Biological energy interrelationships and glossary of energy terms. Pubi.Natl. Acad. Sci. Nat. Res. Counc. U.S., 1411:1-35.Heezen, B.C. and G.L. Johnson. 1969. Alaskan submarine cables: a struggle with a harshenvironment. Arctic 22:413-424.Heimlich-Boran, J.R. 1988. Behavioural ecology of killer whales (Orcus orca) in thePacific Northwest. Can, J. Zool. 66:565-579.Heimlich-Boran, J.R. 1986. Fishery correlation with the occurance of killer whales ingreater Puget Sound. Pp. 113-134, in: B.C. Kirkevold, B.C. and J.S. Lockard (eds.),Behavioural biology of killer whales. Alan R. Liss, New York.Hemmingsen, A.M. 1960. Energy metabolism as related to body size and respiratorysurfaces, and its evolution. Reports of the Steno Memorial Hospital and NordinskInsulin Laboratorium 9:6-110.Hertel, H. 1966. Structure, form, movement. Reinhold, New York.Heyning, J.E. 1988. Presence of solid food in a young killer whale. (Orcinus orca).Marine Mammal Science 4:68-7 1.Heyning, J.E., and M.E. Dahiheim. 1988. Orcinus orca. Mammalian Species 304: 1-9.Heyning, J.E. and M.E. Dahiheim (in press). Killer Whales. In: S.H. Ridgway and R.J.Harrison (eds.), Handbook of marine mammals, Vol. 6.Hewlett, G. 1970. Skana undergoes breathalizer test. VPA Newsletter Vol. XIV (Jan.-Feb.).Hill, A.V. 1950. The dimensions of animals and their muscular dynamics. Science Progress38: 209-230.Hoerner, S.F. 1965. Fluid-dynamic drag. S.F. Hoerner, Midland Park, N.J.Hoyt, E. 1990. Orca the whale called killer. Camden House, Ont.129Innes, S., and D.M. Lavigne. 1991. Do cetaceans really have elevated metabolic rates?Physiol. Zool. 64:1130-1134.limes, S., D.M. Lavigne, W.M. Earle and KM. Kovacs. 1987. Feeding rates of seals andwhales. J. of Animal Ecology 56:115-130.Irving, L. 1973. Aquatic Mammals. Pp. 47-96, in. G.C. Whittow (ed.), Comparativephysiology of thermoregulation. Academic Press, New York, N.Y.Irving, L., P.F. Scholander, and S.W. Grinnel. 1941. The respiration of the porpoise,Tursiops truncatus. J. of Cell. and Comp. Physiol. 17:145-168.Johannessen, C.L. and J.A. Harder. 1960. Sustained swimming speeds of dolphins.Science 132:1550-155 1.Jonsgard, A, and P.B. Lyshoel. 1970. A contribution to the knowlegde of the biology ofthe killer whale Orcinus orca (L). Nytt. Bag. Zool. 18:41-48.Kanwisher, J.W., and G. Sundnes. 1965. Physiology of a small cetacean. Pp. 45-53, in:Universitetets Institutt for Mann Biologi and Statens Institutt for Hvalforskning (ed.),Hvalradets Skrifter. Universiteteforlaget, Oslo.Kanwisher, J.W., and G. Sundnes. 1966. Thermal regulation in cetaceans. Pp. 397-409,in: K.S. Norris (ed.), Whales, dolphins, and porpoises. University of California Press,Berkeley, CA.Kastelein, R.A. and R. van Battum. 1990. The relationship between body weight andmorphological measurements in Harbour porpoises (Phocoenaphocoena) from theNorth Sea. Aquatic Mammals 16:48-52.Kastelein, R.A. and N. Vaughan. 1989. Food consumption, body measurements andweight changes of a female killer whales, (Orcinus orca). Aquatic Mammals 15:18-21.Kastelein, R.A., J. Ford, E Berghout, P.R. Wiepkema, and M. van Bosel. 1994. Foodconsumption, growth and reproduction of Belugas (Deiphinapterus leucas) in humancare. Aquatic Mammals 20:81-97.Kastelein, R.A., J. McBain, B. Neurohr, M. Mohri, S. Saijo, I. Wakabayashi, and P.R.Wiepkema. 1993. The food consumption of Commerson’s dolphins (Cephalorynchuscommersonhl). Aquatic Mammals 19:99-121.130Kasting, N.W., S.A. Adderly, T. Safford, and K.G. Hewlett. 1989. Thermoregulation inbeluga (Deiphinapterus leucas) and killer (Orcinus orca) whales. Physiol. Zool.62:687-701.Kawamura, A. 1974. Food and feeding ecology in the southern sei whale. Pp. 25-144, in:The scientific reports of the Whales Research Institut. Tokyo, Japan.Kawamura, A. 1975. A consideration of an available source of energy and its cost forlocomotion in fin whales with special reference to the seasonal migrations. Sci. Rept.Whales Res. Inst. 27:61-79.Kleiber, M. 1987. The fire of life. R.E. Krieger Publishing Co., Malabare, Florida.Kooyman, G.L., D.H. Kerem, W.B. Campbell and J.J. Wright. 1973. Pulmonary gasexchange in a freely diving Weddell seal. Respir. Physiol. 17:283.Kruse, S. 1991. The interactions between killer whales and boats in Johnstone Strait, B.C.Pp. 149-160, in: K. Pryor and K.S. Norris (eds.), Dolphin Societies. University ofCalifornia Press, Berkeley, CA.Kshatriya, M. and R.W. Blake. 1988. Theoretical model of migration energetics in theblue whale, Balaenoptera musculus. J. Theor. Biol. 133:479-498.Lang, T.G. 1975. Swimming, power, and drag measurements of dolphins and porpoises.In: T.Y.T. Wu, C.J. Browkaw, and C. Brennen (eds.), Swimming and flying in nature,Vol. 2. Plenum Press, New York.Lang, T.G. 1966. Hydrodynamic analysis of cetacean performance. Pp. 410-434, in: K.S.Norris (ed.), Whales, dolphins, and porpoises. University of California Press, Berkeley,CA.Lang, T.G. and K. Pryor. 1966. Hydrodynamic performance of porpoises (Stenellaattenuata). Science 152:531-533.Laurie, A.H. 1933. Some aspects of respiration in blue and fin whales. Discovery Rept.7:363.Lavigne, D.M., S. Innes, G.A.J. Worthy, KM. Kovacs, O.J. Schmitz and J.P. Hickie1986. Metabolic rates of seals and whales. Can. J. of Zool. 64:279-284.Lavigne, D.M., W. Varchard, S. Innes and N.A. Oritsland. 1982. Pinniped bioenergetics.In: Mammals in the sea. FAO Fisheries Series 5, Rome, 6:191-235.131Leatherwood, S., K. Goodrich, A.L. Kinter, and R.M. Truppo. 1982. Respiration patternsand ‘sightability’ of whales. Rep. mt. Whal. Commn. 32:601-613.LeBoeuf, B.J., D.E. Crocker, S.B. Blackwell, P.A. Morris, and P.H. Thorson. 1993. Sexdifferences in diving and foraging strategies of northern elephant seals. Symp. Zool.Soc. Lond. 66: 149-178.Lenfant, C., D.W. Kenney, and C. Aucutt. 1968. Respiratory function in the killer whaleOrcinus orca (Linnaeus). Am. J. ofPhysiol. 215:1506-1511.Lockyer, C. 1981 a. Growth and energy budgets of large baleen whales from the southernhemisphere. In: Mammal in the sea, Vol. 3. FAO Fisheries Series No. 5, Rome. 379-487.Lockyer, C. 198 lb. Estimates of growth and energy budget for the sperm whale, Physetercatadon. Pp. 489-504, In: Mammal in the sea, Vol. 3. FAO Fisheries Series #5, Rome.Matkin, CO. 1988. Status of Prince William Sound killer whales and the sablefish fisheryin late 1987. Unpubi. Rep. to Univ. of Alaska, Se Grant Marine Adv. Program.Cordova, Alaska. 10 pp.McAlister, W.B. 1981. Estimates of fish consumption by marine mammals in the easternBering Sea and Aleution Island Area. Report to the NMFS, NOAA, Seattle WA. 89pp.McNab, B.K. 1980. Food habits, energetics, and the population biology of mammals.Amer. Naturalist 116:106-124.McNab, B.K. 1986. The influence of food habits on the energetics of eutherian mammals.Ecological Monographs 56:1-19.Murie, D.J. 1987. Experimental approaches to stomach content analyses of piscivorousmarine mammals. In: A.C. Huntley, D.P. Costa, G.A.J. Worthy, and M.A. Castellini(eds.), Approaches to marine mammal energetics. Soc. Marine Mammal., Special Publ.No.1, 127-145.Nichol, L.M. 1990. Seasonal movements and foraging behaviour of resident killer whales(Orcinus orca) in relation to the inshore distribution of salmon (Onchorynchus spp.) inB.C. M.Sc. Thesis, University of B.C., Vancouver, B.C.Norberg, B. and D.E. Bain. 1994. Implementation and assessment of the Acoustic Barrierat the Hiram M. Chittenden Locks using calibrated measurements of the sound field.NMFS Report.132Norris, K. S. 1961. Standardized methods for measuring and recording data on the smallercetaceans. J. Mammal. 42:471-476.Norris, K. S. and J. Prescott. 1961. Observations on Pacific cetaceans of Californian andMexican waters. Univ. Calif. Pub!. Zoo!. 63:291-401.Olesiuk, P.F., M.A. Bigg and G.M. Ellis. 1990a. Life history and population dynamics ofresident killer whales (Orcinus orca) in the coastal waters of British Columbia andWashington State. Rep. mt. Whal. Commn. 12:209-243.Olesiuk, P.F., M.A. Bigg and G.M. Ellis. 1990b. Recent trends in the abundance ofharbour seals, Phoca vitulina, in British Columbia. Can. J. of Fish. & Aqu. Sc. 47:992-1003.Olsen, C.R., R. Elsner, F.C. Hale, and D.W. Kenney. 1969. HBlowh of the pilot whale.Science 163:953-955.Olsen, C.R., F.C. Hale, and R. Elsner. 1969. Mechanics of ventilation in the pilot whale.Resp. Physiol. 7:137-149.Oritsiand, N.A. and K. Ronald. 1975. Energetics of the free-diving harp seals (Phocagroenlandica). Rapp. P.-V. Reun. CIEM 169:451-454.Osborne, R.W. 1986. A behavioural budget of Puget Sound killer whales. Pp. 211-250,in: B.C. Kirkevold and J.S. Lockard (eds.) Behavioural biology of killer whales. AlanR. Liss, New York.Parry, D.A. 1949. The swimming of whales and discussion of Grays Paradox. J. Exptl.Biol. 26:24-34.Perez, M.A., and E.E. Mooney. 1986. Increased food and energy consumption oflactating northern fur seals (Callorhinus ursinus). Fish. Bull. 84:371.Perez, MA., W.B. McAlister, and E.E. Mooney. 1990. Estimated feeding rate relationshipof marine mammals based on captive animal data. NOAA Tech. Memorandum NIvIFSF/NWC- 184.Peters, R.H. 1989. The ecological implications of body size. Cambridge University Press,Cambridge, MA. 329 pp.Pike, R.L. and M.L. Brown. 1975. Nutrition: an integrated approach. John Wiley andSons Inc., Toronto, Ontario.133Prange, H.D. 1976. Energetics of swimming of a sea turtle. J. Exptl. Biol.64:1-12.Prange, H.D. and K. Schmidt-Nielsen. 1970. The metabolic cost of swimming in ducks. J.Exptl. Biol. 53:763-777.Purves, P.E. 1963. Locomotion in whales. Science 197:334-337.Ray, R.D., J.D. Upson and B.J. Henderson. 1977. A systems approach to behavior, III:Organismic pace and complexity in time-space fields. Psychol. Rec. 27:649-682.Ray, R,R,, ML. Carison, M.A. Carison, T.M. Carison, and J.D. Upson. 1986.Behavioural and respiratory synchronization quantified in a pair of captive killerwhales. Pp. 187-210, in.. B.C. Kirkevold and J.S. Lockard (eds.), Behavioural biologyof killer whales. Alan R. Liss, New York.Reddy, M., T. Kamolnik, D. Skaar, C. Curry and S.H. Ridgway. 1991. Bottlenosedolphins: energy consumption during pregnancy, lactation, and growth. Presented atthe IMATA Conference, Vallejo, CA. 1991.Reeves, R.R., and E. Mitchell. 1987. Cetaceans of Canada. Communications Directorate,DFO, Ottawa, Ontario.Rice, D.W. 1968. Stomach contents and feeding behavior of killer whales in the easternNorth Pacific. Norsk Hvalfanst-Tidende 2:35-38.Rice, D.W. and A.A. Wolman. 1971. The life history and ecology of the grey whale(Eschrichtius robustus). Amer. Soc. Mammal., Spec. Pubi. No. 3.Ridgway, S.H., B.L. Scronce and J. Kanwisher. 1969. Respiratory function and deepdiving in a bottlenose porpoise. Science 166:1651-1652.Ridgway, S.H. 1972. Mammals of the sea: biology and medicine. Charles C. Thomas,Springfield, Illinois.Ridgway, S.H., and R.J. Harrison. 1986. Diving dolphins. Pp. 33-58, in. M.M. Bryden,and R. Harrison (eds.), Research on dolphins. Clarendon Press, Oxford.Schmidt-Nielsen, K. 1972. Locomotion: Energy cost of swimming, flying and running.Science 177:222-228.Schmidt-Nielsen, K. 1984. Scaling. Cambridge University Press, Cambridge, MA.134Schmidt-Nielsen, K. 1990. Animal physiology: adaptation and environment. CambridgeUniversity Press, Cambridge, MA.Schmitz, O.J. and D.M. Lavigne. 1984. Intrinsic rate of increase, body size, and specificmetabolic rate in marine mammals. Oecologia 62:305-309.Scholander, P.F. 1940. Experimental investigations on the respiratory function in divingmammals and birds. Hvalradets Skr. 22: 1-32.Sergeant, D.E. 1969. Feeding rates of cetacea. FiskDir. Skr. Ser. HavUnders. 15:246-258.Shapunov, V.M. 1973. Food requirements and energy balance in the Black SeaBottlenose Dolphin (Tursiops truncatusponticus Barabasch). In: K.K. Chapskii andV.E. Sokolov (eds.), Morphology and ecology of marine mammals; seals, dolphins andporpoises. John Wiley and Sons, New York, N.Y.Shapunov, V.M. 1973. Evaluation of the economy and effectiveness of externalrespiration in the dolphin Phocoenaphocoena. J. Evol. Biochem. & Physiol. 7:331-336.Slijper, E.J. 1979. Whales. Cornell University Press, Ithaca, N.Y.Spencer, M.P., T.A. Gornall, and T.C. Poulter. 1967. Respiratory and cardiac activity ofkiller whales. J. Appl. Physiol. 22:974-98 1.Stahl, W.R. 1967. Scaling of respiratory variables in mammals. J Appi. Physiol. 22:453-460.Stevens, G.A. 1950. Swimming of dolphins. Science Progress 3 8:524-525.Sugarman, P., and A. Shepard. 1984. Field guide to the orca whales. The Whale Museum,Friday Harbor, WA.Sumich, J.L. 1986. Latitudinal distribution, calf growth and metabolism, and reproductiveenergetics of gray whales, Eschrichtius robustus. Ph.D. thesis, Oregon StateUniversity, Corvallis, OR.Sumich, J.L. 1983. Swimming velocities, breathing patterns, and estimated costs oflocomotion in migrating gray whales, Eschrichtius robustus. Can. J. Zool. 6 1:647-652.Sverdrup, H.V., M.W. Johnson and R.H. Fleming. 1946. The oceans. Prentice Hall, NewYork.135Taylor, C.R., K. Schmidt-Nielsen and J.L. Raab. 1970. Scaling of energetic cost ofrunning to body size in mammals. Amer. J. Physiol. 219:1104-1107.Taylor, C.R., N.C. Heglund, and G.M.O. Maloiy. 1982. Energetics and mechanics ofterrestrial locomotion. J. Exptl. Biol. 97:1-2 1.Thomas, G.L. and F.L. Felleman. 1988. Acoustic measurements of the fish assemblagebeneath killer whale pods in the Pacific Northwest. Pp.276-284, in: J. Sigurjonssonand S. Leatherwood (eds.), North Atlantic killer whales. Rit Fiskideildar, J. MarineRes. Inst., Reykjavik.Thompson, D., A.R. Hiby, and M.A. Fedak. 1993. How fast should I swim? Behaviouralimplications of diving physiology. Symp. zool. Soc. Lond. 66:349-368.Thompson, D.A. 1961. On growth and form. Cambridge University Press, Cambridge,UK.Tucker, V.A. 1970. Energetic cost of locomotion in animals. Comp. Biochem. Physiol34:841-846.Tucker, V.A. 1975. The energetic cost of moving about. Amer. Scientist 63: 413- 419.U.S. Dept. of Commerce. 1986. Tide tables 1986, West Coast of North and SouthAmerica. NOAA., Riverdale, MD.U.S. Dept. of Commerce. 1987. Tide tables 1986, West Coast of North and SouthAmerica. NOAA, Riverdale, IVID.Vogel, S. 1988. Life’s devices. Princeton University Press, Princeton, N.J.Wahrenbrock, E.A., G.F. Maruschak, R. Eisner, and D.W. Kenney. 1974. Respiration andmetabolism in two baleen whale calves. Mar. Fish. Rev. 36:3-9.Waite, J.M. 1988. Alloparental behaviour in killer whales, Orcinus orca. M.Sc. thesis,University of California, Santa Cruz, CA.Walker, L.A., L. Cornell, K.D. Dahi, N.M. Czekala, C.M. Dargen, B. Joseph, A.J.W.Hsueh, and B.L. Lasley. 1988. Urinary concentrations of ovarian steroid hormonemetabolites and bioactive follicle-stimulating hormone in killer whales (Orcinus orca)during ovarian cycles and pregnancy. Biol. Reprod. 39:1013-1020.Webb, P.W. 1975. Hydrodynamics and energetics of fish propulsion. Bulletin of theFisheries Res. Board of Canada, Bull. 190, 158 pp.136Wenzel, F. and R. Sears. 1988. A note on killer whales in the Gulf of St. Lawrence,including an account of an attack on a minke whale. Pp. 202-204, in: J. Sigurjonsson,and S. Leatherwood (eds.), North Atlantic killer whales. Rit Fiskideildar, J. MarineRes. Inst., Reykjavik.Williams, T.M. 1983. Locomotion in the North American mink, a semi-aquatic mammal. J.Exptl. Biol. 103:155-168.Williams, T.M. 1989. Swimming by sea otters: adaptations for low energetic costlocomotion. J. Comp. Physiol. A 164:815-824.Williams, T.M., and G.L. Kooyman. 1985. Swimming performance and hydrodynamiccharacteristics of harbor seals Phoca vilulina. Physiol. Zool.58:576-589.Williams, T.M., J.E. Haun, W.A. Friedi, R.W. Hall, and L.W. Bivens. 1991. Assessing thethermal limits of bottlenose dolphins: a cooperative study by trainers, scientists, andanimals. Pp. 89-98, in: S. Allen (ed), Proc. Intl. Marine Animal Trainers Assoc.Conf., Vallejo, CA.Williams, T.M., W.A. Friedl, M.L. Fong, R.M. Yamada, P.Sedivy, and J.E. Haun 1992.Travel at low energetic cost by swimming and wave-riding bottlenose dolphins.Nature 355:821-823.Williams, T.M., W.A. Friedl, J.E. Haun and N.K. Chun. 1993 a. Balancing power andspeed in bottlenose dolphins (Tursiops truncalus). Symp. zoo!. Soc. Lond. 66:383-394.Williams, T.M., WA. Fried! and J.E. Haun. 1993 b. The physiology of bottlenose dolphins(Tursiops truncatus): heart rate, metabolic rate and plasma lactate concentrationduring excercise. J. Exptl. Biol. 179:31-46.Worthy, G. A.J. 1991. Thermoregulatory implications of the interspecific variation inblubber composition of odontocete cetaceans. Abstract presented at the 9th BiennialConference on the Biology of Marine Mammals, Chicago, Ill.Worthy, G.A.J. 1990. Nutritional energetics for marine mammals. Pp. 489-520, in: L.A.Dierauf (ed.), CRC handbook of marine mammals medicine: health, disease, andrehabilitation. CRC Press. Boca Raton.Worthy, G.A.J. and E.F. Edwards. 1990. Morphometric and biochemical factors affectingheat loss in a small temperate cetacean (Phocoenaphocoena) and a small tropicalcetacean (Stenella attenuata). Physiol. Zool. 63:432.137Worthy, G.A.J., S. Innes, B.M. Braune, and R.E.A. Stewart. 1987. Rapid acclimation ofcetaceans to an open-system respirometer. In: A.C. Huntley, D.P. Costa, G.A.J.Worthy, and M.A. Castellini (eds.), Approaches to marine mammal energetics. Soc.for Marine Mammalogy, Special PubI. No.1, 115-126.Wuersig, B., F. Cipriano, and M. Wuersig. 1991. Dolphin movement patterns: informationfrom radio and theodolite tracking studies. Pp. 79-112, in: K. Pryor and K.S. Norris(eds.), Dolphin societies. Univ. California Press, Berkeley, CA.Wunder, B.A, 1975. A model for estimating metabolic rates of active or resting mammals.J. Theoret. Biol. 49:345-3 54.Yasui, W.Y. and D.E. Gaskin. 1986. Energy budget of a small cetacean, the harbourporpoise, Phocoena phocoena (L.). Ophelia 25:183-197.Zar, J.H. 1984. Biostatistical analysis. Prentice Hall, Englewood Cliffs, N.H.138


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