Open Collections

UBC Theses and Dissertations

UBC Theses Logo

UBC Theses and Dissertations

Effects of temperature on the repeat swimming performance, metabolic rates and swimming economy of salmonids… MacNutt, Meaghan J. 2003

Your browser doesn't seem to have a PDF viewer, please download the PDF to view this item.

Item Metadata

Download

Media
831-ubc_2003-0584.pdf [ 4.11MB ]
Metadata
JSON: 831-1.0090958.json
JSON-LD: 831-1.0090958-ld.json
RDF/XML (Pretty): 831-1.0090958-rdf.xml
RDF/JSON: 831-1.0090958-rdf.json
Turtle: 831-1.0090958-turtle.txt
N-Triples: 831-1.0090958-rdf-ntriples.txt
Original Record: 831-1.0090958-source.json
Full Text
831-1.0090958-fulltext.txt
Citation
831-1.0090958.ris

Full Text

EFFECTS OF TEMPERATURE O N THE REPEAT SWIMMING PERFORMANCE, METABOLIC RATES A N D SWIMMING E C O N O M Y OF SALMONIDS (ONCORHYNCHUS SPP.) by MEAGHAN J. MACNUTT B.Sc., Acadia University, 2001 A thesis submitted in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE in the F A C U L T Y OF G R A D U A T E STUDIES (Department of Zoology) We accept this thesis as conforming to the required standard THE UNIVERSITY OF BRITISH C O L U M B I A September, 2003 © Meaghan J. MacNutt, 2003 In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the head of my department or by his or her representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. Department of 7^  f)0 OQ V The University of British Columbia Vancouver, Canada Date 7 A r f rW 2f)02> DE-6 (2/88) Thesis abstract The primary goal of this research was to predict how changes in water temperature affect the swimming performance and energetic cost of transport in adult pink salmon (Oncorhynchus gorbuscha) and sockeye salmon (O. nerka), thus contributing to their ability to reach natal streams and spawn successfully. The prolonged swimming performance (U c r j t ) , minimum and maximum metabolic rate (Mo2-min and Mo2-m ax), ar>d oxygen cost of transport (COT) for upper Fraser River pink salmon were assessed across a range of naturally occurring temperatures using Brett-type swim tunnel respirometers and compared with values for sockeye salmon. To reduce mortality in senescing fish we minimized holding time and, therefore, thermal acclimation to as little as 48 hours before experiments. Therefore, we also used a salmonid model, the cutthroat trout (O. clarki clarki), to examine the effects of 48-hour and 3-week temperature acclimation periods on U c r i t . The length of the acclimation period had no significant effect on either the first or second U c r j t or on the recovery ratio (the quotient of Ucrit-2/UCrit-i)- These results indicate that a 48-h acclimation to experimental temperatures may be sufficient in studies of swimming performance with this species. Contrary to previous beliefs, pink salmon were capable of similar relative critical swimming speeds as sockeye salmon (2.25 FL-s') , but sockeye salmon swam to a higher absolute U c r i l (125.9 cm-s"1) than pink salmon (116.4 cm-s"1) because of their larger size. However, some individual pink salmon swam faster than all the sockeye salmon tested. Metabolic rate increased exponentially with swimming speed (P < 0.01) in both species and was higher for pink than sockeye salmon (P = 0.01), although swimming efficiency (was not significantly different between the species at their optimal swimming speeds minimum cost of transport; C O T m i n ) . The upper and lower limits of metabolism also increased exponentially with temperature (Mo 2 m i n P = 0.01; M o 2 m a s , P < 0.01, respectively) but were not different between species (Mo 2 m i n P = 0.93; M o 2 m a x , P = 0.38). The relationship between M o 2 and swimming speed was positively affected by temperature in pink salmon (P = 0.01), but average and minimum C O T s were independent of temperature over the range tested (9-22 e C ) in both species. Overall, a higher degree of inter-individual variability and thermal insensitivity in pink salmon suggest that this species might not be as locally adapted to particular upriver migrations as are sockeye salmon. ii Table of contents Thesis abstract ii Table of contents iii List of tables v List of tables vi Acknowledgements vii Chapter 1. Thesis overview and brief literature review 1 Introduction of thesis topic 1 Introduction to fish swimming and energetics 3 Evaluating swimming performance 4 Evaluating energy use 7 Effects of temperature on swimming performance and energy use 9 Thesis objectives 10 Literature cited 13 Chapter 2. The effect of temperature and acclimation period on repeat swimming performance in cutthroat trout (Oncorhynchus clarki clarki) 21 Abstract ; 21 Introduction .'...22 Materials and Methods 23 Study animals 23 Evaluating swimming performance 24 Data analysis and statistics 25 Results 26 Discussion ''. 29 Effect of acclimation period 29 Effect of temperature on swimming performance 30 Effect of temperature on recovery ratio 31 Conclusion 32 Acknowledgements 32 Literature cited 34 Chapter 3. Effects of temperature on swimming performance, energetics and aerobic capacities of adult migrating pink salmon {Oncorhynchus gorbuscha): a comparison with sockeye salmon (O. nerka) 38 Abstract 38 Introduction 39 Materials and Methods 41 Study animals 41 Evaluating swimming performance 43 Evaluating energy use 44 Video analyses 45 Data analysis and statistics 45 Results 4 7 Swimming performance 47 Metabolic variables 49 Recovery from exhaustive exercise 50 Energetic cost of swimming 50 Discussion 53 Swimming performance 53 Metabolic variables and cost of transport 55 Potential relevance of inter-individual variability 58 Conclusion 59 Acknowledgements 60 Literature cited 61 Appendix 65 Chapter 4. Summary and Potential Ecological Relevance of Conclusions 67 Thesis summary 67 Potential implications of species differences in inter-individual variation 69 Literature cited 71 iv List of tables Table 2.1. Critical swimming speeds ( U c r i t - i and U c r j , . 2 ) and recovery ratios (U c r i t _2 /U C r i t - i ) of cutthroat trout that performed repeat U c r i t tests after either a 48-hour or 3-week acclimation to experimental temperatures. . 26 Table 3.1. Estimated aerobic cost of swimming a distance equivalent to the entire upriver migration for upper Fraser River pink and early Stuart sockeye salmon. Calculations are based on the mean minimum and average costs of transport for each species. 53 Table A3.1. Critical swimming speeds of adult pink and sockeye salmon that performed repeat ramp 20-minute UCRIT tests. Trial 1 and Trial 2 (U c r i t_i and U c r i t_2 respectively) were separated by a 45-minute recovery at 0.45 FL-s \ Recovery ratio (RR) is the quotient of U C ri t-2 /U c r i t . i . The speed of gait transition from steady caudal fin swimming to consistent burst-coast swimming (UGT) is presented as a percent of UCRIT. 65 v List of figures Figure 2.1. Critical swimming speeds (FL-s"1) of cutthroat trout that performed repeat Ucrit tests. Data from both acclimation groups are pooled at each experimental temperature. There is a positive relationship between Ucrit-i (•) and experimental temperature, but the increasing trend of U c r i t . 2 (o) with increasing temperature is not significant. Symbols represent means ± S.E. Numbers represent N value for each group. 28 Figure 2.2. Recovery ratios (U c ri t. 2/U c r i t.i) for cutthroat trout that performed repeat U c r i t tests. Horizontal line at 1.0 indicates equal performance on first and second U c r i t trials. Symbols represent means + S. E . Numbers represent N value for each group. Asterisk indicates temperature at which recovery ratio was different from unity (P=0.04). ; 29 Figure 3.1. Map of British Columbia, Canada showing the Fraser River watershed with sampling locations (stanHell's Gate; Y: Yale, B: BC Hydroelectric Dam), testing sites (C: Cultus Lake, B: BC Hydroelectric Dam, S: Simon Fraser University) and potential spawning grounds of upper Fraser River pink salmon (solid circle: Seton River; solid oval: Thompson River) and early Stuart sockeye salmon (broken oval). 42 Figure 3.2. Maximum critical swimming speed for pink salmon (o, —) and sockeye salmon (•, —) in (A) FL-s"1 and (B) cm-s"1. The quadratic curve of best fit is shown for each species with 95% confidence intervals. 48 Figure 3.3. (A) Minimum (o pink salmon; • sockeye salmon) and maximum (• pink salmon; • sockeye salmon) rates of oxygen consumption of fish performing repeat U c r i t tests at a range of naturally occurring temperatures and (B) the resulting aerobic metabolic scope (Scope = M o 2 . m a x - Mo2-min; ° pink salmon; • sockeye salmon). 49 Figure 3.4. Rate of oxygen consumption at intermediate swimming speeds of Trial 1 (A) and Trial 2 (B) for pink (o) and sockeye salmon (•). 51 Figure 3.5. Costs of transport at intermediate swimming speeds for pink (N = 23) and sockeye salmon (N = 9). (A) Total cost of transport includes both the cost of swimming and the costs associated with standard or resting metabolism. (B) Net cost of transport excludes the resting metabolic rate and represents the energy spent only swimming. 52 Figure 3.6. (A) Tail beat frequencies measured at intermediate swimming speeds for pink (o N = 20) and sockeye salmon (• N = 10). (B) Oxygen consumption rates associated with given tail beat frequencies. 54 vi Acknowledgements First of all I would like to thank Scott Hinch for being such an accessible and approachable advisor. Even at his busiest, Scott always has time for his students. Tony Farrell is a wealth of knowledge, enthusiasm and passion for research. I thank him for asking tough questions and challenging me. Scott and Tony's respective strengths and areas of expertise complemented each other to provide me with great leadership and support. I also greatly appreciate Trish Schulte for joining my committee in full swing and offering fresh perspectives and ideas. Without a great deal of field and lab assistance my research would have been impossible. The ever-cheerful Andrew Lotto, with his knowledge of the people, places and fishes of the Fraser River, was indispensable to me. I especially thank Andrew for being a champion shelter-builder, and for getting us all up and down the road to Hell's Gate safely. Much appreciation to Jamie Phibbs for being a great fish swimmer/tail beat counter and for knowing when to leave the country so I could get some work done. Also to Stephanie Topp for her positive attitude and expertise in First Aid. Very special thanks to Chris Lee for showing me the ropes in the beginning and offering lots of help and advice along the way. I'm grateful for countless discussions with Glenn Crossin and Steve Cooke, who were both extremely helpful in getting ideas sorted out and onto paper. Many thanks also to Yuho Okada and Richard Anderson for their help in the field and lab. I would also like to thank the staff at the Fisheries and Oceans Lab in Cultus Lake, especially Bryan Smith and Dave Barnes for their complete willingness to answer questions and provide technical assistance. Thanks so much to friends and family that have made this a great experience, especially everyone that has belonged to, or been affiliated with, the Hinch Lab during the past two years. I sincerely could not have asked for a better group of people to work with. Finally I would like to thank Drs. Dan Toews and Tom Herman from Acadia University who inspired my fascination with both physiology and ecology. Without their encouragement to pursue a graduate degree I would not have done so. vii Chapter 1. Thesis overview and brief literature review Introduction of thesis topic Functions such as locomotor performance capacity evolve over time, provided they are selected upon and possess inter-individual variability, repeatability, and heritability (Bennett 1990). These attributes have been shown in various taxa, demonstrating that locomotor ability can adapt in response to different environmental pressures. For example, faster burst speeds in coho salmon (Oncorhynchus kisutch) conveyed a selective advantage over slower swimmers (Taylor and McPhail 1985), and speed has been linked to predator avoidance in iguanas (Christian and Tracy 1981). Burst speed and maximal exertion were shown to vary within a population of garter snakes (Thamnophis sirtalis) (Jayne and Bennett 1990) and such variability has been shown to be repeatable in several studies on fish (Kolok 1999). Performance is heritable in garter snakes (Garland 1988; Jayne and Bennett 1990), thoroughbred race horses (Langlois 1980), and lizards (Scleroporus occidentalis) (vanBerkum and Tsuji 1987). Both aerobic and anaerobic metabolic capacities have been linked to forms of locomotor performance (Bennett 1991) and it is therefore plausible that locomotory energetics have also evolved within a species over time. Semelparous Pacific salmon (Oncorhynchus spp.) serve as an excellent model for examining evolutionary questions about swimming energetics. During the up-river spawning migration, Pacific salmon do not feed and therefore rely solely on body energy reserves to complete the energetically expensive migration, sexual maturation, and spawning behaviours (Brett 1995). Inappropriate allocation of stored body energy due to inefficient migration limits the amount of energy available for reproductive tissues, and may compromise the quality and viability of gametes. Due to their restrictive energy budget, the ability to swim at or near energetically optimal speeds may be under strong natural selection in Pacific salmon (Hinch and Rand 2000). This suggests that swimming ability and aerobic capacity may evolve in response to environmental pressures imposed by the spawning migration. This selective pressure may be especially strong for females due to the higher energy requirements of eggs relative to sperm. Swimming may become more economical due to depressed standard metabolic rates, improved gas transport, cardiac function, or hydrodynamic morphology, or by superior swimming strategies and behaviour. Such enhancements would allow species to minimize energy use per unit distance or per unit time. 1 Of interest to the ecological or evolutionary physiologist are questions concerning the divergence or convergence of phenotypes (i.e. swimming performance or metabolism) in response to different selective pressures. For example, does variation in the distance and difficulty of migrations undertaken by different salmon populations effect stock differences in swimming ability and aerobic capacity? Questions of optimality also dominate these fields. Has each salmon stock evolved to function optimally, with peak swimming performance and energetic efficiency, at temperatures most commonly encountered in river? More pragmatically, Pacific salmon are important in Canada for political, economical, ecological and cultural reasons. However, the sustainability of healthy and abundant salmon stocks is not guaranteed. Since 1996, extreme river temperatures and flows, poor fish health and changes in migration timing have contributed to large increases in en route and pre-spawning mortality in many Fraser River salmon stocks (Macdonald 2000; Macdonald et al. 2000; Lapointe 2002). Although historical trends in Pacific salmon abundance are not clear (Finney et al. 2000), current stock declines are of great concern to managers, scientists, fishers and others. In order to develop management plans to deal with these problems, the threat of changing river conditions on salmon migration success must first be evaluated. This requires precise quantification of swimming energetics to determine the impact of changing temperature and flow regimes on the ability to complete the upriver migration and spawn successfully within the energy budget. Based on work with sockeye salmon (O. nerka) (Crossin 2002; Lee et al. 2003a; Lee et al. 2003b), it has become clear that managers must understand the implications of changing river conditions for each population (as well as each species) so that management plans can be customized to reflect stock-specific differences. This thesis will examine the swimming energetics of the "long-distance" migrating stocks of sockeye and pink salmon. Some sockeye salmon stocks undertake the longest upriver migrations (eg early Stuart) and are assumed to be the strongest swimmers of all the Fraser River salmon (Burgner 1991). Conversely, pink salmon (O. gorbuscha) generally migrate less than half the distance upriver compared with early Stuart sockeye and are considered the poorest swimmers of all the Pacific salmon (Heard, 1991). Early Stuart sockeye migrate approximately 1089 km upriver to an.elevation of more than 701 m, while upper Fraser pink salmon (spawning either in Seton or Thompson River) migrate approximately 323 km and ascend 401 m. Therefore, a 2 comparison of these stocks should demonstrate any range of variability that exists between the two highest performing populations of Fraser River pink and sockeye salmon. Introduction to fish swimming and energetics Understanding how fish swim requires a multidisciplinary examination of the physical, physiological and behavioural aspects of movement through an aquatic medium. Many experimental and theoretical studies have examined the biomechanical (Webb 1984; Rome et al. 1993), morphological (Brett 1965; Wardle 1977; Webb 1977; Weihs 1977; Arnold 1983), and hydrodynamic (Weihs 1973; Fuiman and Batty 1997) elements of fish swimming. Many others have attempted to tease apart the physiological components concerning the muscular (Bone et al. 1978; Rome 1994), respiratory (Beamish 1964a, 1964b; Beamish and Mookherjii 1964; Brett 1973; Kiceniuk and Jones 1977; Farrell and Daxboeck 1981; Jobling 1994; Stevens et al. 1998), neural (Grillner and Kashin 1976), and cardiovascular (Smith et al. 1967; Randall and Daxboeck 1982; Keen and Farrell 1994; Farrell et al. 1996; Steffensen and Farrell 1998) systems. These reductionist studies have been crucial to our understanding of the fundamentals of fish swimming, but they provide little practical information about how well an organism is able to survive in its environment. It is not the physical and physiological mechanisms that are of interest to the ecologist, rather the resultant swimming abilities and associated energetic costs under various environmental conditions. Three main categories of swimming have been described, based on the duration of the activity and the speed attained by the fish. Sustained swimming occurs at speeds that can be maintained indefinitely without fatigue. For the purposes of evaluating swimming performance, continuous swimming for greater than 200 minutes indicates a sustained swimming speed. Fish commonly swim at sustained speeds during migration, as well as during routine activities such as foraging and station holding (Beamish 1978). Sustained swimming involves primarily red muscle fibres and is essentially an aerobically fuelled activity. Power supplied by the muscles matches the metabolic demand, and waste production is balanced by elimination (Jones 1982). At the other extreme, sprinting, or burst swimming is an entirely anaerobic activity involving fast-twitch white muscle fibres. These high speeds can rapidly exhaust the intracellular energy supply and result in fatigue in less than twenty seconds (Jones 1982). Burst activity is of ecological importance because it facilitates predator avoidance, capture of prey and the navigation of rapid 3 currents (Beamish 1978). Intermediate swimming speeds that can be maintained for between 20 seconds and 200 minutes are considered prolonged speeds (Beamish 1978). Although prolonged swimming is primarily fuelled aerobically, as swimming speed increases within this category the relative contribution of the anaerobic energy system increases (Jones 1982). Evaluating swimming performance Researchers have developed numerous ways to assess the performance of burst, prolonged and sustained swimming under both laboratory and field conditions. Field techniques range from simply marking an individual and measuring the amount of time required to travel a gauged distance (Beamish 1978) to the use of sophisticated biotelemetry to measure swimming speed and tail beat frequency (Videler and Weihs 1982; McKinley and Power 1992; Hinch et al. 1996; Booth et al. 1997; Hinch and Rand 1998). In the laboratory, much emphasis has been placed on designing swimming chambers, flumes and tunnels to enable more precise measurements of swimming performance (Fry and Hart 1948; Blazka et al. 1960; Priede and Holloday 1980; Steffensen et al. 1984; Gehrke et al. 1990). Relatively little effort has been invested in examining the burst swimming abilities of fish. Techniques tend to be simple and fairly imprecise as they often consist of chasing fish around in tanks and measuring swimming speeds over very short time intervals (Goolish 1991). More sophisticated approaches using raceways and fishways (Collins et al. 1962; Schwalme et al. 1985) have been attempted but far more interest has been shown in the evaluation of prolonged and sustained swimming. Swimming tunnels designed by Brett (1964) and Blazka (1960) have become the most commonly used tools in examining the primarily aerobic swimming capacities of fish. Although different by design, both the Brett-type and Blazka-type swim tunnels allow precise control of a relatively consistent, rectilinear velocity profile (Blazka et al. 1960; Brett 1964). Hence, researchers can measure the ability of a single fish, or groups of fish, to swim at known speeds. Of particular interest to researchers is a specific prolonged velocity known as critical swimming speed, or U c r i t . U c r j t is the maximum swimming speed that can be maintained for a given period of time and is measured using variations of the increased velocity test originally described by Brett (1964). Protocol for the commonly named "U c rit test" involves forcing a fish to swim in an increasing current field until the fish is fatigued and no longer able to maintain station in the 4 swimming tunnel. Water velocity (and therefore swimming speed) is increased incrementally, with each velocity interval maintained for a predetermined amount of time (Hammer 1995). Critical swimming speed can then be calculated as: U c r i t = U c + (tf/ti X Ui) where U c is the velocity of the last fully completed interval, tf is amount of time completed before fatigue in the final interval, tj is the length of each interval, and Ui is the velocity increment (Brett 1964). Brett originally defined U c rit as the maximum speed that could be maintained for 60 minutes and therefore the protocol for measuring Ucrjt(60) used 60 minute intervals. Subsequent researchers have used intervals ranging from two to 75 minutes, but it is currently accepted that 15-20 minute steps are sufficient to accurately measure U c r i t (Hammer 1995). Velocity increments have also varied substantially and have been expressed in absolute terms (cm/s), relative terms (body lengths/s) or as a fraction of U c rit (Hammer 1995). Several studies have examined the effects of varying velocity increments and interval times with contrasting results (Jones 1971; Farlinger and Beamish 1977). It seems logical however, that results are comparable only across studies using similar protocols. A recent variation of the traditional U c r i t test was developed by Jain et al. (1997) to decrease the time required to assess Ucrit- This new "ramp U c r i t test" uses shorter time intervals (~5 min) until approximately 50-75% of the estimated U c r i t is reached, at which point longer intervals (-20-30 min) at each swimming speed commence. Providing that (1) a brief practice swim is performed during the habituation period, (2) swimming at the end of the ramp period does not require a significant anaerobic contribution and (3) at least two full-length time intervals are completed, the ramp U c r i , protocol has been shown to accurately estimate U c r j t in rainbow trout (O. mykiss). It appears that long periods of swimming at low speeds are not necessary to accurately assess U c r ; t . These aerobically fuelled swimming speeds can be maintained more-or-less indefinitely and do not contribute to the fatigue associated with the completion of a U c r i t test (Jain et al. 1997). Theoretical support for the ramp U c r i t protocol was presented by Burgetz et al (1998) who showed that anaerobic metabolism (measured as the accumulation of intramuscular lactate) does not occur until swimming at 70% of U c r j t and is not a significant fuel source until 80% of U c r i t is reached. 5 The ability to repeatedly perform exhaustive exercise is an ecologically relevant measure because it assesses the ability to cope with recurring challenges, as might be encountered during an upriver migration or when repeatedly escaping predators. Accordingly, some authors force fish to perform repeated U c r j t tests in order to measure the recovery ratio (RR) (Jain et al. 1998; Tierney 2000; Lee et al. 2003a; Farrell et al. 2003). RR (U c r i t . 2 /U c r i t - i ) ) is the proportion of maximum performance that can be attained on the second trial when an exhaustive challenge is repeated. Repeat swimming tests offer advantages in that repeated measures analyses help to circumvent the typically large individual variation in swimming performance that might confound statistical analysis of single measurements. In addition to maximum prolonged speed, investigators are also interested in swimming endurance. Endurance, or time to fatigue at a given swimming speed, is measured using fixed velocity tests. After an acclimation period, swimming speed is either gradually or abruptly increased to the test velocity and the time required for the fish to fatigue is measured. Endurance is usually measured on groups of fish at several sub-maximal speeds (Hammer 1995). Upon plotting endurance against swimming speed, the resultant fatigue curve demonstrates the boundaries between burst, prolonged and sustained swimming. Fatigue curves can then be used to compare performance of different species or sizes of fish, or performance under different environmental conditions. For these reasons, fatigue curves are an important tool in the study of fish swimming (Peake et al. 1997). Fixed velocity tests also allow mean maximum sustained speed (somewhat of an analogue to U c rj t) to be calculated as the velocity at which 50% of a test group of fish have fatigued. There are advantages and disadvantages to both increased (Ucrj,) and fixed velocity (endurance) tests. Endurance tests take a great deal more time and require much larger sample sizes of physiologically similar fish than U c r i t tests. The advantage, however, is that fish become exhausted under stable physiological conditions, unlike U c r i t tests which exhaust fish over constantly changing physiological conditions. Therefore the two testing methods measure different forms of exhaustion and are not directly comparable (Hammer 1995). Another commonly measured swimming parameter is tail beat frequency (TBF) (Bainbridge 1958, Herskin & Steffensen 1998, Hunter & Zweifel 1971). In salmonids, thrust is generated by undulatory movements of the body and caudal fin (Webb 1984). The amplitude of these tail beats 6 remains fairly constant across cruising speeds (Bainbridge 1958), but it has been shown repeatedly that, except at very slow swimming speeds, a linear relationship exists between swimming speed and tail beat frequency (TBF) (Hunter and Zweifel 1971; Williams and Brett 1987; Leonard et al. 2000). Measuring T B F can be as simple as observing a swimming fish's body movements (as in the study discussed in Chapter 2), or as sophisticated as using electromyogram (EMG) telemetry to determine the rate of muscle contraction. Using the latter method, T B F can be measured at a very fine time scale, allowing researchers to evaluate costs of activities like migrating (Hinch and Rand 1998; Hinch et al. 2003). Furthermore, the development of inter- and intra-specific relationships between swim speed-TBF and swim speed-M02 facilitate a shortcut to assigning costs of swimming in the field (Hinch et al. 1996). These relationships also allow the calculation of stride length, the distance the fish is propelled forward by each tail beat. In body-caudal fin swimmers like salmon, maximum stride length has been shown to range between 0.6 and 0.8 times the length of the fish, regardless of fish size (Wardle 1975). Comparisons of stride lengths across populations or species reveal information about differential power production by swimming musculature (Hinch and Rand 2000). In general, stride length is a reasonable measure of the physical aspects of swimming efficiency. Evaluat ing energy use In addition to determining attainable and sustainable swimming speeds, researchers are often also interested in the energetic cost of activity for fish. Metabolic rates (MR) at rest and during activity are commonly measured in association with U c r i t testing using indirect calorimetry, or respirometry (Ferrannini 1988). Swim tunnels can often be sealed off to serve as respirometers, allowing whole body gas exchange to be measured via changes in oxygen and carbon dioxide in the water. Since the amount of CO2 released by a fish is often negligible compared to the amount of bound CO2 normally found in water, measurements of oxygen uptake alone are considered sufficient to determine metabolic rate (Braefield 1985). Metabolic rate is generally stated in terms of oxygen consumption, or M02 (mg O2 consumed/unit body mass/unit time). However, if so desired, M R can also be transformed into calories using the oxycalorific equivalent of 3.25 cal/mg 0 2 (Brett 1985). 7 Several types of metabolism must be considered when discussing swimming energetics. Standard metabolic rate (SMR; the equivalent of basal M R in endotherms) is the rate of energy use by a fasting, non-reproductive fish at complete rest (Adams and Breck 1990). This is seldom measured however, due to the difficulties of keeping fish motionless and unstressed during testing. Standard metabolic rate has also been determined by extrapolating Mo2-swimming speed curves back to zero activity (Brett and Glass 1973; Williams et al. 1986). However, this method may underestimate S M R because it does not consider that fish may be capable of reallocating available oxygen to meet the demands of the working muscle when swimming begins (Farrell et al. 2003). Indeed, it has been shown in chinook salmon (O. tshawytscha) that oxygen consumption does not always increase when a fish begins swimming (Gallaugher et al. 2001). Therefore measurements of routine metabolic rate (RMR), recorded while a fish is calm, motionless and in the post-absorptive state, often serve as a proxy for standard metabolic rate. R M R gives an indication of basic metabolic requirements, and influences all other metabolic rates (Brett 1995). Activity metabolic rate measures oxygen consumption at various levels of activity, i.e. at various swimming speeds. It allows the calculation of aerobic cost of transport (COT; mg O2 kg"1 km"1), at intermediate swimming speeds. In turn, the energetically optimal cruising speed at which cost of transport is minimized (U o p t ) can be determined. Active metabolic rate (AMR) is a measure of maximum aerobic capacity. It is generally assumed that this maximum oxygen consumption (M02 m a x) occurs at U c r i t (Farrell and Steffensen 1987). This physiological limit determines the metabolic threshold between sustained activities (cruising) and burst swimming, and is therefore of ecological importance. Any activity with energy demands beyond the active M R cannot be maintained indefinitely and will result in the accumulation of oxygen debt (Brett 1995). Metabolic scope (MS; mg O2 kg"1 min"1) is the difference between A M R and S M R and is a measure of the oxygen available for aerobic work at any given time. A large metabolic scope is desirable because it increases the range of activity that can be fuelled without incurring any oxygen debt (Priede 1985). The ability to recover quickly from exhaustive exercise is also extremely important ecologically because it minimizes 'wasted' time spent resting and may enhance predator avoidance (Priede 1977; Jain et al. 1997). Time to recovery can be derived from an excess post-exercise oxygen consumption (EPOC) curve recorded following exhaustive exercise. 8 Although the locomotor and metabolic capacities of many fish species and age classes have been studied extensively (Brett 1964; Beamish 1981; Claireaux and Lagardere 1999; Jordan et al. 2001), relatively little research has been conducted on the swimming performance and metabolism of sexually mature salmon. Difficulties arise when handling and holding these moribund fish, and senescing salmon often do not respond well to the stress of exercise testing. However, a few authors have studied the swimming abilities, energetics and behaviour of sexually mature salmon on spawning migration (Milliken 1983; Williams et al. 1986; Williams and Brett 1987; Hinch et al. 1996; Crossin 2002; Hinch et al. 2002; Lee et al. 2003a; Standen et al. 2002), laying the groundwork for research conducted towards this thesis. These works will be discussed in greater depth in Chapter 3. Effects of temperature on swimming performance and energy use in fish The literature dedicated to the effects of temperature on exercise and energy use in fish is vast, including several comprehensive reviews of the subject (Fry 1947; Houston 1982; Bennett 1990; Randall and Brauner 1991; Taylor et al. 1996; Kieffer 2000). Therefore I have included only a very brief summary of the effects of temperature on fish swimming and energetics. Temperature is the principle rate-controlling factor in the aquatic environment and affects physiological processes at the cellular and molecular levels of organization. Through its effects on the properties of water, temperature also impacts fishes indirectly by changing viscosity and oxygen availability (Houston 1982). For these reasons, water temperature is considered the most significant controlling abiotic factor in the lives of fishes (Fry 1971). From Antarctica to the Amazon, fish occupy niches with environmental temperatures ranging from -1.9 to 42 °C (Franklin 1998) and temperatures encountered by individuals, populations or species of fish can rise and fall several degrees daily, seasonally or geographically. Even the most stenothermal of fishes, including upriver migrating salmon often encounter highly variable temperatures, with daily fluctuations in some systems of up to 13° C (Mochan and Mrazik 2000). It is therefore a persistent struggle for fish to not only survive, but to maintain function in the face of changing temperature conditions, whether these changes occur in a matter of seconds or thousands of years. Fish can compensate for acute thermal changes by either altering behaviour (seeking refugia) or physiology (changing chemical reaction rates) (Schreer and Cooke 2002). At 9 a longer time scale, further physical and physiological changes can occur which allow fish to acclimate or adapt to chronic thermal conditions (Fry 1947). The effects of temperature on the swimming performance and metabolism of teleost fish have been examined extensively. Although proximate temperature effects on biochemistry, cardiac function, gas transport and muscle contractility can be complex and ambiguous, the ultimate effects of temperature on swimming performance and energetics are relatively consistent across fish species. It has been shown repeatedly, and in different species, that U c r j t , oxygen consumption and metabolic scope all increase with warming to an optimum temperature, beyond which these variables begin to decrease (Fry and Hart 1948; Griffiths and Alderdice 1972; Rome et al. 1990; Keen and Farrell 1994; Claireaux et al. 2000). Brett and Glass (1973) showed that this optimum occurs at 1 5 ° C for juvenile sockeye salmon, while juvenile coho salmon (O. kisutch) have been shown to perform optimally at 2 0 ° C (Griffiths and Alderdice 1972). I am unaware of any work on the effects of temperature on swimming performance or energetics of pink salmon. Thesis objectives The primary goal of this research was to predict how changes in water temperature affect the swimming performance and energetic cost of transport in adult migrating pink and sockeye salmon, thus contributing to their ability to reach their natal streams with sufficient remaining energy to spawn successfully. Collected data has contributed to improving the predictive capability of an existing sockeye bioenergetics model (Rand and Hinch 1998) and will allow the development of a much-needed model for pink salmon. Such models are valuable because they predict migration success and allow managers to set appropriate escapement targets in the face of changing environmental conditions. Given important differences in the life history of pink and sockeye salmon, my second goal was to relate interspecific differences in swimming performance and energetics (or lack thereof) to observed differences in ecology and behaviour between the two species. In order to meet these objectives we evaluated the prolonged swimming performance (20-minute U c r i t ) and oxygen consumption (at rest, at intermediate swimming speeds, at U c r i t , 45-minutes 10 post-exercise) of long distance migrating pink and sockeye salmon. However, performing swimming respirometry with senescing Pacific salmon did not prove to be an easy task. To reduce mortality we minimized fish holding time, but as a result thermal acclimation was restricted to as little as 48 hours before experiments. Thus, a third objective became to determine whether there were any effects of an abbreviated thermal acclimation period on swimming performance and energy use in Pacific salmon. A salmonid model (and congener to pink and sockeye salmon) the cutthroat trout (O. clarki clarki) was used to meet this objective but due to technical problems we were unable to evaluate energy use in swimming cutthroat trout. Due to its relevance in the interpretation of other data in this thesis, this thesis will first address this objective. In summary, the thesis objectives were: 1. To determine whether a minimum of 48 hours acclimation to experimental temperature facilitates salmonid swimming performance comparable to when experimental temperature equals ambient, fully acclimated temperature 2. To evaluate and compare the impact of changing water temperature on the swimming abilities (U c ri t, RR) and metabolic parameters (RR, R M R , A M R , M S , COT) of pink and sockeye salmon 3. To discuss the inter-specific comparison of swimming abilities and metabolic parameters in the context of observed differences in life history and migration experiences between pink and sockeye salmon It was expected that brief exposure to experimental temperature would allow only partial thermal acclimation to occur, and thus critical swimming speed might be impaired in fish that acclimated for only 48 hours as compared to 3 weeks. The extent of the reduction in swimming performance caused by incomplete thermal acclimation was unknown. It was predicted that swimming performance and energy efficiency would be optimal at a species-specific temperature that is normally encountered during spawning migrations. Because early Stuart sockeye salmon encounter a broader range of temperatures during upriver migration than do upper Fraser River pink salmon it was expected that sockeye salmon might be better able 11 to compensate for changing temperature and measured parameters would show less temperature dependence in this species. These objectives are addressed in the following two chapters, which are written as stand-alone manuscripts to be submitted to peer-reviewed journals. The final chapter summarizes the major findings of the thesis and discusses the potential ecological and evolutionary relevance of the conclusions. 12 Literature cited Adams, S. M . and Breck, J. E . (1990). Bioenergetics. In Methods for Fish Biology. Edited by C . B. Schreck and P. B. Moyle. American Fisheries Society, Bethesda, Maryland, U S A . pp. 389-415. Arnold, S. J. (1983). Morphology, performance and fitness. American Zoologist 23: 347-361. Bainbridge, R. (1958). The speed of swimming of fish as related to size and to the frequency and amplitude of the tail beat. Journal of Experimental Biology 35: 109-133. Beamish, F. W . H . (1964a). Respiration of fishes with special emphasis on standard oxygen consumption II. Influence of weight and temperature on respiration of several species. Canadian Journal of Zoology 42: 177-188. Beamish, F. W. H . (1964b). Respiration of fishes with special emphasis on standard oxygen consumption III. Influence of oxygen. Canadian Journal of Zoology 42: 355-366. Beamish, F. W. H . (1978). Swimming Capacity. In Locomotion. Edited by W. S. Hoar and D. J. Randall. Academic Press, New York. pp. 101-187. Beamish, F. W. H . (1981). Swimming performance and metabolic rate of three tropical fishes in relation to temperature. Hydrobiologia 83: 245-254. Beamish, F. W. H . and Mookherjii, P. S. (1964). Respiration of fishes with special emphasis on standard oxygen consumption I. Influence of weight and temperature on respiration of goldfish, Carassius auratus L . Canadian Journal of Zoology 42: 161-175. Bennett, A . F. (1990). Thermal dependence of locomotor capacity. American Journal of Physiology 259: R253-R258. Bennett, A . F. (1991). The evolution of activity capacity. Journal of Experimental Biology 160: 1-23. Blazka, P., Volf, M . and Cepela, M . (1960). A new type of respirometer for the determination of the metabolism of fish in an active state. Physiologia Bohemoslovenica 9: 553-558. Bone, Q., Kiceniuk, J. and Jones, D. (1978). On the role of the different fibre types in fish myotomes at intermediate swimming speeds. Fishery Bulletin U.S. 76: 691-699. Booth, R. K. , McKinley, R. S., Okland, F. and Sisak, M . M . (1997). In situ measurement of swimming performance of wild Atlantic salmon (Salmo salar) using radio transmitted electromyogram signals. Aquatic Living Resources 10: 213-219. Braefield, A . E . (1985). Laboratory Studies of Energy Budgets. In Fish Energetics: New Perspectives. Edited by P. Calow. Croom Helm Ltd., Sydney, Australia, pp. 257-282. Brett, J. R. (1964). The respiratory metabolism and swimming performance of young sockeye salmon. Journal of the Fisheries Research Board of Canada 21: 1183-1226. 13 Brett, J. R. (1965). The relation of size to rate of oxygen consumption and sustained swimming speed of sockeye salmon {Oncorhynchus nerka). Journal of the Fisheries Research Board of Canada 22: 1491-1501. Brett, J. R. (1973). Energy expenditure of sockeye salmon, Oncorhynchus nerka, during sustained performance. Journal of the Fisheries Research Board of Canada 30: 1799-1809. Brett, J. R. (1985). Correction in use of oxycalorific equivalent. Canadian Journal of Fisheries and Aquatic Science 42: 1326-1327. Brett, J. R. (1995). Energetics. In Physiological Ecology of Pacific Salmon. Edited by C. Groot, W. C. Clarke and L. Margolis. UBC Press, Vancouver, pp. 1-68. Brett, J. R. and Glass, N . R. (1973). Metabolic rates and critical swimming speeds of sockeye salmon {Oncorhynchus nerka) in relation to size and temperature. Journal of the Fisheries Research Board of Canada 30: 379-387. Burgetz, I. J., Rojas-Vargas, A., Hinch, S. G. and Randall, D. J. (1998). Initial recruitment of anaerobic metabolism during sub-maximal swimming in rainbow trout (Oncorhynchus mykiss). Journal of Experimental Biology 201: 2711-2721. Burgner, R. L. (1991). Life History of Sockeye Salmon (Oncorhyncus nerka). In Pacific Salmon Life Histories. Edited by C. Groot and L. Margolis. UBC Press, Vancouver, BC, Canada, pp. 3-117. Christian, K. A . and Tracy, C. R. (1981). The effect of the thermal environment on the ability of hatchling Galapagos land iguanas to avoid predation during dispersal. Oecologia 49: 218-223. Claireaux, G. and Lagardere, J.-P. (1999). Influence of temperature, oxygen and salinity on the metabolism of the European sea bass. Journal of Sea Research 42: 157-168. Claireaux, G., Webber, D. M . , Lagadere, J.-P. and Kerr, S. R. (2000). Influence of water temperature and oxygenation on the aerobic metabolic scope of Atlantic cod (Gadus morhua). Journal of Sea Research 44: 257-265. Collins, G. B., Elling, C. H. and Gauley, J. R. (1962). Ability of salmonids to ascend high fishways. Transactions of the American Fisheries Society 91: 1-7. Crossin, G. T. (2002). Effects of ocean climate and upriver migratory constraints on the bioenergetics, fecundity, and morphology of wild, Fraser River salmon. M.Sc. thesis, University of British Columbia, Vancouver. Farlinger, S. and Beamish, F. W. H. (1977). Effects of time and velocity increments on the critical swimming speed of largemouth bass (Micropterus salmoides). Transactions of the American Fisheries Society 106: 436-439. Farrell, A . P. and Daxboeck, C- (1981). Oxygen uptake in the lingcod, Ophidon elongatus, during progressive hypoxia. Canadian Journal of Zoology 59: 1272-1275. Farrell, A. P. and Steffensen, J. F. (1987). An analysis of the energetic costs of the branchial and cardiac pumps during sustained swimming. Fish Physiology and Biochemistry 4: 73-79. 14 Farrell, A . P., Gamperl, A . K . , Hicks, J. M . T. , Shiels, H . A . and Jain, K . E . (1996). Maximum cardiac performance of rainbow trout {Oncorhynchus mykiss) at temperatures approaching their upper lethal limit. Journal of Experimental Biology 199: 663-672. Farrell, A . P., Lee, C . G . , Tierney, K . , Hodaly, A . , Clutterham, S., Healey, M . C . , Hinch, S. G . and Lotto, A . (2003). Field-based measurements of oxygen uptake and swimming performance with adult Pacific salmon using a mobile respirometer swim tunnel. Journal of Fish Biology 62: 64-84. Ferrannini, E . (1988). The theoretical bases of indirect calorimetry: a review. Metabolism 37: 287-301. Finney, B. P., Gregory-Eaves, I., Sweetman, J. , Douglas, M . S. V . and Smol, J . P. (2000). Impacts of climate change and fishing on Pacific salmon abundance over the past 300 years. Science 290: 795-799. Franklin, C. E . (1998). Studies of evolutionary temperature adaptation: muscle function and locomotor performance in Antarctic fish. Clinical and Experimental Pharmacology and Physiology 25: 753-756. Fry, F. E . J. (1947). Effects of the environment on animal activity. University of Toronto Studies, Biological Series 55: 1-62. Fry, F. E . J. (1971). The effects of environmental factors on the physiology of fish. In Fish Physiology. Edited by W. S. Hoar and D. J. Randall. Academic Press, New York. pp. 1-98. Fry, F. E . J. and Hart, J . S. (1948). Cruising speed of goldfish in relation to water temperature. Journal of the Fisheries Research Board of Canada 7: 169-175. Fuiman, L . A . and Batty, R. S. (1997). What a drag it is getting cold: partitioning the physical and physiological effects of temperature on fish swimming. Journal of Experimental Biology 200: 1745-1755. Gallaugher, P., Thorarensen, H . , Kiessling, A . and Farrell, A . P. (2001). Effects of high intensity exercsie training on cardiovascular function, oxygen uptake, internal oxygen transfer and osmotic balance in chinook slamon {Oncorhynchus tsawytscha) during critical speed swimming. Journal of Experimental Biology 204: 2861-2872. Garland, T. (1988). Genetic basis of activity metabolism. I. Inheritance of speed, stamina, and antipredator displays in the garter snake Thamnophis sirtalis. Evolution 42: 335-350. Gehrke, P. C , Fidler, L . E . , Mense, D. C . and Randall, D. J. (1990). A respirometer with controlled water quality and comptuerized data acquisition for experiments with swimming fish. Fish Physiology and Biochemistry 8: 61-67. Goolish, E . M . (1991). Aerobic and anaerobic scaling in fish. Biological Reviews 66: 33-56. Griffiths, J. S. and Alderdice, D. F. (1972). Effects of acclimation and acute temperature experience on the swimming speed of juvenile coho salmon. Journal of the Fisheries Research Board of Canada 29: 251-264. 15 Grillner, S. and Kashin, S. (1976). On the generation and performance of swimming in fish. In Neural control of locomotion. Edited by R. Herman, S. Grillner, P. S. G . Stein and D. G . Stuart. Plenum Press, New York. pp. Hammer, C . (1995). Fatigue and exercise tests with fish. Comparitive Biochemistry and Physiology 112A: 1-20. Hinch, S. G . and Rand, P. S. (1998). Swim speeds and energy use of upriver-migrating sockeye salmon (Oncorhynchus nerka): role of local environment and fish characteristics. Canadian Journal of Fisheries and Aquatic Science 55: 1821-1831. Hinch, S. G . and Rand, P. S. (2000). Optimal swimming speeds and forward-assisted propulsion: energy-conserving behaviours of upriver-migrating adult salmon. Canadian Journal of Fisheries and Aquatic Science 57: 2470-2478. Hinch, S. G. , Standen, E . M . , Healey, M . C . and Farrell, A . P. (2002). Swimming patterns and behaviour of upriver migrating adult pink (Oncorhynchus gorbuscha) and sockeye (O. nerka) salmon as assessed by E M G telemetry in the Fraser River, British Columbia, Canada. Hydrobiologia 483: 147-160. Hinch, S. G . , Diewert, R. E . , Lissimore, T . J. , Prince, A . M . J. , Healey, M . C. and Henderson, M . A . (1996). Use of electromyogram telemetry to assess difficult passage areas for river-migrating adult sockeye salmon. Transactions of the American Fisheries Society 125: 253-260. Houston, A . H . (1982). Thermal effects upon fishes. Publication of the Environmental Secretariat. No. 18566. Hunter, J. R. and Zweifel, J . R. (1971). Swimming speed, tail beat frequency, tail beat amplitude, and size in jack mackerel, Tracharus symmetricus, and other fishes. Fishery Bulletin 69: 253-266. Jain, K. E . , Hamilton, J. C . and Farrell, A . P. (1997). Use of a Ramp Velocity Test to Measure Critical Swimming Speed in Rainbow Trout. Comparitive Biochemistry and Physiology 117A: 441-444. Jain, K. E . , Birtwell, I. K . and Farrell, A . P. (1998). Repeat swimming performance of mature sockeye salmon following a brief recovery period: a proposed measure of fish health and water quality. Canadian Journal of Zoology 76: 1488-1496. Jayne, B. C. and Bennett, A . F. (1990). Selection on locomotor performance capacity in a natural population of garter snakes. Evolution 44: 1204-1229. Jobling, M . (1994). Respiration and Metabolism. In Fish Bioenergetics. Edited by M . Jobling. pp. 121-145. Jones, D. R. (1971). The effect of hypoxia and anaemia on the swimming performance of rainbow trout (Salino gairdneri). Journal of Experimental Biology 55: 541-551. Jones, D. R. (1982). Anaerobic exercise in teleost fish. Canadian Journal of Zoology 60: 1131-1134. 16 Jordan, A . D., Jungersen, M . and Steffensen, J. F. (2001). Oxygen consumption of East Siberian cod: no support for the emtabolic cold adaptation theory. Journal of Fish Biology 59: 818-823. Keen, J. E . and Farrell, A . P. (1994). Maximum prolonged swimming speed and maximum cardiac performance of rainbow trout, Oncorhynchus mykiss, acclimated to two different water temperatures. Comparitive Biochemistry and Physiology 108A: 287-295. Kiceniuk, J. W. and Jones, D. R. (1977). The oxygen transport system in trout (Salmo gairdneri) during sustained exercise. Journal of Experimental Biology 69: 247-260. Kieffer, J. D. (2000). Limits to exhaustive exercise in fish. Comparitive Biochemistry and Physiology 126A: 161-179. Kolok, A . S. (1999). Interindivudal variation in the prolonged locomotor performance of ectothermic vertebrates: a comparison of fish and herpetofaunal methodologies and a broad review of the recent fish literature. Canadian Journal of Fisheries and Aquatic Science 56: 700-710. Langlois, B. (1980). Heritability of racing ability in thoroughbreds - a review. Livestock Production Science 7: 591-605. Lee, C . G. , Farrell, A . P., Lotto, A . , MacNutt, M . J. , Hinch, S. G . and Healey, M . C . (2003a). The effect of temperature on swimming performance and oxygen uptake in adult sockeye {Oncorhynchus nerka) and coho {O. kisutch) salmon stocks. Journal of Experimental Biology. 206: 3239-3251. Lee, C . G. , Farrell, A . P., Lotto, A . , Hinch, S. G . and Healey, M . C . (2003b). Excess post-exercise oxygen consumption in adult sockeye {Oncorhynchus nerka) and coho {O. kisutch) salmon stocks following critical speed swimming. Journal of Experimental Biology 206: 3253-3260. Leonard, J. B., Leonard, D. R. and Ueda, H . (2000). Active metabolic rate of masu salmon determined by respirometry. Fisheries Science 66: 481-484. Macdonald, J. S. (2000). Mortality during the migration of Fraser River sockeye salmon {Oncorhynchus nerka): a study of the effect of ocean and river environmental conditions in 1997. Canadian Technical Report of Fisheries and Aquatic Sciences 2315. Fisheries and Oceans Canada. Burnaby, B C . Macdonald, J. S., Foreman, M . G . G . , Farrell, T. , Williams, I. V . , Grout, J . , Cass, A . , Woodey, J. C , Enzenhofer, H . , Clarke, W. C , Houtman, R., Donaldson, E . M . and Barnes, D. (2000). The influence of extreme water temperatures on migrating Fraser River sockeye salmon {Oncorhynchus nerka) during the 1998 spawning season. Canadian Technical Report of Fisheries and Aquatic Sciences 2326. Fisheries and Oceans Canada. Burnaby, B C . McKinley, R. S. and Power, G . (1992). Measurement of activity and oxygen consumption for adult lake sturgeon (Acipenser fulvescens) in the wild using radiotransmitted E M D signals. In Wildlife telemetry: remote monitoring and tracking of animals. Edited by I. G . Priede and S. M . Swift. Ellis Horwood, West Sussex, U K . pp. 307-318. 17 Milliken, C . (1983). Study of the metabolic rate in relation to swimming speed of adult pink salmon from the Fraser and Thompson Rivers. Contract OSB83-00375. Department of Fisheries and Oceans. Bamfield, B C . Mochan, D. G . and Mrazik, S.. (2000). A summary of chemistry, temperature, habitat and macroinvertebrate data from the Southeast Oregon ambient monitoring sites (1992-1998). Technical Report. BIO00-03. Peake, S., Beamish, F. W . H., McKinley, R. S., Scruton, D. A . and Katopodis, C . (1997). Relating swimming performance of lake sturgeon, Acipenser fulvescens, to fishway design. Canadian Journal of Fisheries and Aquatic Science 54: 1361-1366. Priede, I. G . (1977). Natural selection for energy efficiency and relationship between activity level and mortality. Nature 267: 610-611. Priede, I. G . (1985). Metabolic Scope in Fishes. In Fish Energetics: New Perspectives. Edited by P. Tytler and P. Calow. Croom Helm Ltd., pp. 33-63. Priede, I. G . and Holloday, F. G . T. (1980). The use of a new tilting tunnel respirometer to investigate some aspects of metabolism and swimming activity of the plaice (Pleuronectes platessa L.). Journal of Experimental Biology 85: 295. Rand, P. S. and Hinch, S. G . (1998). Swim speeds and energy use of upriver-migrating sockeye salmon {Oncorhynchus nerka): simulating metabolic power and assessing risk of energy depletion. Canadian Journal of Fisheries and Aquatic Science 55: 1832-1841. Randall, D. J. and Daxboeck, C . (1982). Cardiovascular changes in the rainbow trout (Salmo gairdneri) during exercise. Canadian Journal of Zoology 60: 1135-1140. Randall, D. J. and Brauner, C . (1991). Effects of environmental factors on exercise in fish. Journal of Experimental Biology 160: 113-126. Rome, L . C . (1994). The mechanical design of the fish muscular system. In Mechanics and Physiology of Animal Swimming. Edited by L . Maddock, Q. Bone and J. M . V . Rayner. Cambridge University Press, pp. Rome, L . C , Funke, R. P. and Alexander, R. M . (1990). The influence of temperature on muscle velocity and sustained performance in swimming carp. Journal of Experimental Biology 154: 163-178. Rome, L . C , Swank, D. and Corda, D. (1993). How fish power swimming. Science 261: 340-343. Schreer, J. F. and Cooke, S. J. (2002). Behavioural and physiological responses of smallmouth bass to a dynamic thermal environment. American Fisheries Society Symposium 31: 191-203. Schwalme, K. , Mackay, W. C . and Linder, D. (1985). Suitability of vertical slot and Denil fishways for passing north-temperate, non-salmond fish. Canadian Journal of Fisheries and Aquatic Science 42: 1815-1822. 18 Smith, L . S., Brett, J. R. and Davis, J . C . (1967). Cardiovascular dynamics in swimming adult sockeye salmon. Journal of the Fisheries Research Board of Canada 24: 1775-1789. Standen, E . M . , Hinch, S. G . , Healey, M . C . and Farrell, A . P. (2002). Energetic costs of migration through the Fraser River Canyon, British Columbia, in adult pink (Oncorhynchus gorbuscha) and sockeye (O. nerka) salmon assessed by E M G telemetry. Canadian Journal of Fisheries and Aquatic Science 59: 1809-1818. Steffensen, J. F. and Farrell, A . P. (1998). Swimming performance, venous oxygen tension and cardiac performance of coronary-ligated rainbow trout, Oncorhynchus mykiss, exposed to progressive hypoxia. Comparitive Biochemistry and Physiology 119A: 585-592. Steffensen, J. F., Johansen, K . and Bushnell, P. G . (1984). A n automated swimming respirometer. Comparitive Biochemistry and Physiology 79A: 473-476. Stevens, E . D., Sutterlin, A . and Cook, T. (1998). Respiratory metabolism and swimming performance in growth hormone transgenic Atlantic salmon. Canadian Journal of Fisheries and Aquatic Science 55: 2028-2035. Taylor, E . B. and McPhail, J . D. (1985). Variation in burst and prolonged swimming performance of coho salmon, Oncorhynchus kisutch. Transactions of the American Fisheries Society. 42: 2029-2033. Tierney, K . (2000). The repeated swimming performance of sockeye, coho and rainbow trout in varying conditions. M.Sc. thesis, Simon Fraser University, Burnaby, B . C . vanBerkum, F. H . and Tsuji, J . S. (1987). Inter-familial differences in sprint speed of hatchling lizards {Scleroporus occidentalis). J. Zool. Lond 212: 511-519. Videler, J . J. and Weihs, D. (1982). Energetic advantages of burst-and-coast swimming of fish at high speeds. Journal of Experimental Biology 97: 169-178. Wardle, C. S. (1977). Effects of size on the swimming speeds of fish. In Scale Effects in Animal Locomotion. Edited by T. J. Pedley. Academic Press, London, pp. Webb, P. W. (1977). Effects of. size on performance and energetics of fish. In Scale Effects in Animal Locomotion. Edited by T. J. Pedley. Academic Press, London, pp. Webb, P. W. (1984). Form and function in fish swimming. Scientific American 251: 72-82. Weihs, D. (1973). Optimal fish cruising speed. Nature 245: 48-50. Weihs, D. (1977). Effects of size on sustained swimming speeds of aquatic organisms. In Scale Effects in Animal Locomotion. Edited by T. J. Pedly. Academic Press, London, pp. Williams, I. V . and Brett, J. R. (1987). Critical swimming speed of Fraser and Thompson River pink salmon {Oncorhynchus gorbuscha). Canadian Journal of Fisheries and Aquatic Science 44: 348-356. Williams, I. V . , Brett, J. R., Bell, G . R., Traxler, G . S., Bagshaw, J. , McBride, J . R., Fagerlund, U . H . M . , Dye, H . M . , Sumpter, J. P., Donaldson, E . M . , Bilinski, E . , Tsuyuki, H . , Peters, M . D. , 19 Choromanski, E . M , Cheng, J . H . Y . and Coleridge, W . L . (1986). The 1983 early run Fraser and Thompson River pink salmon; morphology, energetics and fish health. Bulletin. XXIII. 20 Chapter 2. The effect of temperature and acclimation period on repeat swimming performance in cutthroat trout (Oncorhynchus clarki clarki) Abstract Hatchery cutthroat trout Oncorhynchus clarki clarki were used as a salmonid model to examine the effects of 48-hour and 3-week temperature acclimation periods on critical swimming speed (U c rit). UCrit was determined for fish at acclimation temperatures of 7, 14 and 18° C using two consecutive ramp U c r i t tests in mobile Brett-type swim tunnels. A n additional group was tested at the stock's ambient rearing temperature of 10° C . The length of the temperature acclimation period had no significant effect on either the first or the second U c r j t (U c rit-i and U c r i t_2, respectively) or on the recovery ratio (the quotient of U c r i t -2 /UCrit-t)- As anticipated, there was a significant positive relationship between U c r it-i and temperature (P<0.01) for both acclimation periods, and an increasing, though non-significant, trend between U c r i t -2 and temperature (P=0.10). Acclimation temperature had no significant effect (P=0.71) on the recovery ratio. These results indicate that a 48-h acclimation to experimental temperatures within the range of -3° C and + 8° C of the acclimation temp may be sufficient in studies of swimming performance with this species. Because cutthroat trout, like other salmonids, occupy thermally variable environments, we suggest that their rapid thermal acclimation to minimize changes to swimming performance and recovery are likely adaptive. 21 Introduction The effects of temperature change on swimming performance have primarily been examined in one of two ways. Fish are swum either at temperatures to which they are acclimated (Fry and Hart 1948a; Beamish 1964; Brett and Glass 1973; Keen and Farrell 1994; Claireaux et al. 2000) or at temperatures to which they are acutely introduced (Fry and Hart 1948b; Peterson and Anderson 1969; Griffiths and Alderdice 1972; Guderley et al. 2001). Both acute and acclimatory increases in temperature have been shown to improve swimming performance by enhancing biochemical reaction rates (Franklin 1998), skeletal muscle contractility (Rome et al. 1990), cardiac performance (Kolok and Farrell 1994a, 1994b) and even hydrodynamics (Fuiman and Batty 1997). However, beyond an optimum, temperature begins to negatively affect swimming performance (Brett 1971), probably through factors such as the breakdown of enzymes necessary for aerobic metabolism (Fry and Hart 1948a), a reduction in cardiac performance (Farrell et al. 1996), and a reduction of oxygen availability (Brett 1971). Given time, salmonids are capable of remarkable degrees of compensation for the proximate effects of high and low temperature on gas transport, and cardiac, biochemical and muscle function (Johnston and Dunn 1987). This acclimation process involves changes in the concentrations and types of enzymes, energy stores, fuel utilization, mitochondrial density, membrane composition, volume of aerobic muscle fibres and patterns of muscle fibre recruitment. Changes associated with thermal acclimation occur on a time course ranging from seconds to several weeks (Johnston and Dunn 1987). For purposes of conducting laboratory experiments, it has been commonly accepted that an acclimation period of 2-3 weeks will allow complete thermal compensation (Houston 1982) with temperature changes often occurring at a rate of 0 .5 -2° C per day (Albers et al. 1983; Beddow et al. 1995), and up to 5° C per day (Venables et al. 1977). However, in nature fish are regularly exposed to a heterogeneous thermal environment and researchers who work with wild fish are therefore never sure that their fish are fully acclimated to the "ambient" conditions in which they are being observed. Even salmonids, which are generally considered stenothermal, are often subjected to substantial daily, seasonal and geographic temperature variability. For example, sockeye salmon {Oncorhynchus nerka) regularly encounter daily changes of 1° C per day and sometimes up to 7° C per day during their spawning migrations in the Fraser River, Canada 22 (Idler and Clemens 1959). Other, smaller salmonid streams have been reported to fluctuate as much as 13° C per day (Mochan and Mrazik 2000). Although complete thermal acclimation is unlikely to occur that rapidly, conservation of functions associated with migration, predation and predator avoidance (i.e. swimming) remains critically important. More recently, it has been shown that the optimum temperature for swimming in adult sockeye salmon is close to that of their natal stream at spawning, despite the fact that the fish may have experienced this temperature for a matter of days at most (Lee et al. 2003a). This raises the question of whether these fish were pre-adapted to this temperature, could acclimate rapidly, or their swimming performance was temperature insensitive over the study's observed range. Another concern is a logistical one. It may be impossible or undesirable to allow a 2-3 week acclimation period because of constraints related to extreme thermal conditions (Cooke et al. 2003) and reproductive development (Burns 1975). In studies of adult salmon, swimming performance is known to fall off as the fish approaches reproductive maturity (Williams et al. 1986), and this concern led Lee et al. (2003a) to use an abbreviated acclimation period for temperature changes of 5° C from ambient. Conversely, Adams and Parsons (1998), who evaluated swimming energetics of smallmouth buffalo (Jctiobus bubalus) only four days post-capture, encouraged other investigators to minimize laboratory acclimation because fish fully acclimated in the laboratory are not physiologically representative of fish acclimatized to similar conditions in the field. In view of the importance of temperature on swimming performance and the uncertainty regarding how brief a thermal acclimation period can be to accommodate the accurate evaluation of these temperature effects, we compared for the first time the effect of a brief (48-hour) and normal (3-week) acclimation period on U c r i t . Tests were performed at three experimental temperatures, which spanned those normally encountered by the model salmonid, the cutthroat trout (Oncorhynchus clarki clarki). Materials and methods S t u d y animals Two year-old (N=42; 400-700 g; 23.5-36.6 cm) cutthroat trout {Oncorhynchus clarki clarki) were obtained from the Fraser Valley Trout Hatchery in Abottsford, British Columbia, Canada 23 where they had been reared in hatchery tanks at approximately 10° C . Fish were placed in two insulated 150 L transport tanks containing ambient hatchery water and were transported 25 minutes by truck to the Fisheries and Oceans Canada laboratory, in Cultus Lake, British Columbia, where they were transferred to three 1200 L tanks. Due to problems with the water delivery system, the majority of fish were held for the first 10 days in hypolimnetic Cultus Lake water at 7° C . Thereafter; water temperature was held at 10° C for an additional 10 days. Subsequently, the fish were sub-divided into seven groups. Six of the groups (each N=6) were exposed to temperatures of 7, 14 or 18° C for a period of either 48 hours or 3 weeks prior to testing their swimming performance. A l l temperature changes occurred in a separate indoor tank at a rate of 1° C-h~\ which was similar to rates of change used in previous studies (Venables et al. 1977). A control group (N=6) remained and was tested at the ambient rearing temperature of 10° C . Fish were fed ad libidum daily on commercial pellets until 48 hours prior to testing. Evaluat ing swimming performance The evening prior to a swim test, a fish was lightly anaesthetized in a 40 L tub containing buffered 0.2 mg-L"1 MS-222 (tricaine methoanosulfonate, Syndel International Inc., Vancouver, Canada). Fork length (FL, cm) and maximum body depth (cm) and width (cm) were measured before introducing the fish to the swim tunnel (described below). The fish recovered in the tunnel for approximately one hour at a water velocity of 0.45 fork lengths per second (FL-s"1) before a practice swim test was performed (Jain et al. 1997). This test entailed increasing water velocity by 0.2 FL-s"1 increments every two minutes until the fish 'failed', or was no longer able to hold station against the water current. Upon failure, water velocity was returned to 0.45 FL-s"1 and the fish was allowed an overnight recovery period of 12-16 h. The following morning, swimming performance was assessed with a repeat ramp-U c r i t test, as described by Jain et al. (1997). Water velocity was increased by increments of 0.2 FL-s"1 at five-minute intervals to a ramp height established by considering both performance on the conditioning test and visual observations of behaviour and performance during the swim trial. This ramp height ranged from 40-150 % of the maximum velocity attained in the practice test, which was equivalent to 48%-100% of the final Ucr i t - Time intervals were then increased to 20 minutes for the remaining velocity increments until fish exhausted. Upon exhaustion, the water velocity was immediately reduced to 0.45 FL-s"1 and the fish was allowed to recover for 45 minutes before performing a second ramp-U c r i t test. 24 U c rit values (FL-s"1) for the first (UCrit-i) a r ) d second (Ucrit-2) swim trials were calculated as in Brett (1964): Ucnt = Uf+ (t/tix U) where Uf is the water velocity of the last fully completed interval (FL-s"1); tf is amount of time spent in the failed interval (min); ti is the length of each interval (20 min); and Uj is the velocity increment (0.2 FL-s"1). Recovery ratio, the quotient of Ucrit-2/UCrit-i, was calculated for each fish. To ensure a constant water temperature and sufficient dissolved oxygen concentration (>7 mg 0-2-L"1), water at the appropriate experimental temperature was continuously delivered to the swim tunnel at a rate of 30 L-min"1 throughout the habituation period and swim test. However, heat generated by the impellor and heat gain by the swim tunnel from ambient air resulted in small increases in the tunnel water temperature during swimming tests ( - 1 ° C). Therefore, the experimental temperatures reported in Table 2.1 reflect those measured at U c r i t . Two Brett-type swim tunnels (471.2 L , internal diameter of swimming chamber (ID)=25.4 cm; and 287.4 L , ID=20.3 cm) were used to conduct tests (Farrell et al. 2003), and this allowed two fish to be tested each day. The cross-sectional area of a fish never exceeded 10% of the cross sectional area of the swimming chamber (mean ± S.E. = 4.0 ± 2.4%) and resulting error due to solid blocking effects (Bell and Terhune 1970) was always less than 10% (3.0 ± 2.6%). Therefore, it was unnecessary to correct swimming speeds for solid blocking effects. Visual observations of the tail and body movements were made whenever possible to identify the swimming speed at which burst-and-coast swimming began to consistently supplement steady body-caudal fin swimming. The speed of gait transition (UGT) was defined as the swimming speed at which a fish displayed three burst/coast sequences (burst to the front of the tunnel followed by passive drifting to the rear of the tunnel) within a one-minute period. Fish often began bursting in response to an initial increase in water velocity, but at low swimming speeds this behaviour was generally restricted to the first minute of an interval. Data analyses and statistics Fish mortality (five fish died in holding tanks before testing, three died in swim tunnel during overnight habituation) reduced the total number available for testing to 34. When using the 25 ramp-U c r i t protocol, measurements of U c r i t are generally considered accurate only if the ramp height is no higher than 50-75% of U c r i t , depending upon the species (Jain et al. 1997) or if fish complete at least two 20-minute intervals before failing. If these criteria are not met, there is a risk of slightly overestimating U c r i t , which can also occur when the protocol involves a very short interval length (Hammer 1995). With our cutthroat trout, 27 out of 34 fish met the required criteria for U c r i t . i . However, more than half the fish failed the second U C n t test before completing two 20-minute intervals, with only 12 fish meeting the criteria for Ucrit-2- In addition, sudden swimming failures were more common among weak swimmers, i.e. those that attained a lower than average U c rit- Therefore, to prevent skewing the data towards stronger swimmers and inflating average U c r i tS, data from all fish was presented and analysed, regardless of whether or not they completed at least two 20-minute intervals before failing. Student t-tests were used to compare fish length between acclimation groups at each temperature and Tukey's H S D test to compare fish length among temperature groupings. Recovery ratio and U Cnt data were analysed using a two-way analysis of variance ( A N O V A ) to test for effects of acclimation period and temperature. In the absence of a significant effect of acclimation length or an interaction of treatment effects, data from both acclimation groups were pooled, data from the 10 .5° C control group were included, and a one-way A N O V A was used to test for the effect of temperature on each response variable. (3 values were calculated to give an indication of the power of each test. Tukey's H S D test was used for post-hoc multiple comparisons of U c rit-1, U c r j t -2, and recovery ratio between temperature groups. A l l differences were considered significant when P<0.05. Analyses were conducted using SPSS 10.0 statistical package (SPSS Science, Chicago, Illinois). Results Allocation of fish to acclimation groups and averages of the response variables are shown in Table 2.1. Fish size and body mass did not differ significantly among the experimental groupings (P>0.05). Consistent burst swimming was initiated at a range of swimming speeds from 55-100% of U c r i t (mean ± S.E. = 83 ± 2 % Ucrit). This suggests fish were swimming normally in the tunnel and is supported by studies on other salmonids that reported the recruitment of white muscle 26 Table 2.1. Critical swimming speeds (Uc r i t_i and Uc ri t_2) and recovery ratios (Uc r i,_2/Uc rj t.i) of cutthroat trout that performed repeat U c r i t tests after either a 48-hour or 3-week acclimation to experimental temperatures. Accl imat ion Group Temperature (° C) 48 hours 3 weeks 10.510.19 3.9810.39 (6) U c r i M (FL-s"1) 8.6±0.11 14.0±0.03 3.32+0.31 (6) 4.19+0.23 (6) 2.8410.50 (4) 4.33+0.51 (5) 18.0±0.03 4.7210.41 (3) 4.4910.57 (4) 10.5+0.19 3.72+0.53 (2) LWztFL-s - 1 ) 8.6+0.11 14.0±0.03 3.0710.37 (6) 3.76+0.39 (6) 2.8410.63 (4) 3.49+0.15 (5) 18.0±0.03 4.3410.47 (3) 3.6410.58 (4) 10.510.19 0.9210.07 (6) Recovery 8.610.11 0.9310.10 (6) 0.9210.07 (4) Ratio 14.010.03 0.8910.07 (6) 0.8210.11 (5) 18.010.03 0.9210.06 (3) 0.9710.01 (4) Values are mean ± s. E- with N in brackets. and anaerobic metabolism at swimming speeds of 50% (Day and Butler 1996), 60% (Lee et al. 2003b) and 70-80% (Burgetz et al. 1998) of U c r i t . A two-way A N O V A identified a significant temperature effect on U c rj t_i (P<0.01), but no effect of acclimation period (P=0.59, (3=0.92) or interaction between treatment effects (P=0.74, (3=0.81). A nearly significant effect of temperature on U c rj t-2 was identified (P=0.06, (3=0.57) but again there was no effect of acclimation period (P=0.71, (3=0.94) or interaction (P=0.96, (3=0.94). Recovery ratio was not affected by temperature (P=0.56, (3=0.14) or acclimation period (P=0.86, (3=0.95), nor was there a significant interaction of main effects (P=0.81, (3=0.92). One-way A N O V A on pooled data indicated that temperature had a significant positive effect on U c rit-i (Figure 2.1; P<0.01). Tukey's test revealed that Ucrit-i was significantly higher for both the 14 and 18° C groups than the 8 .7° C group (P=0.03 and P=0.01 respectively), though the two 27 5 A o Z> 2 ^ 0 0 I I S 10 11 8 10 12 14 16 Temperature (°C) 18 20 Figure 2.1. Critical swimming speeds (FL-s"1) of cutthroat trout that performed repeat U c r j t tests. Data from both acclimation groups are pooled at each experimental temperature. There is a positive relationship between L W i (•) and experimental temperature, but the increasing trend of UCnt-2 (o) with increasing temperature is not significant. Symbols represent means ± S.E. Numbers represent N value for each group. warmer groups were not different from each other or from the control group. Although Ucr[ t-2 also increased with temperature this effect was not significant (Figure 2.1; A N O V A , P=0.10, (3=0.48) and there were no post hoc differences between any of the temperature groups. There was no relationship between recovery ratio and temperature (Figure 2.2; A N O V A , P=0.70, (3=0.87). Despite high (3 values, analyses identified a significant temperature effect on U c r i t - i , and a nearly significant effect on U c rj t_2, indicating that power was sufficient to recognize differences. 28 1.05 -, 1.00 o C\J o => 0.95 0.90 A OC CD > O o CD DC 0.85 -\ 0.80 0 . 7 5 ^ 0.00 0 10 11 * 10 12 14 16 Temperature (°C) 18 20 crit tests. trials. Jcnt Figure 2.2. Recovery ratios (UCnt-2/UCrit-i) for cutthroat trout that performed repeat U , Horizontal line at 1.0 indicates equal performance on first and second U , Symbols represent means ± S. E . Numbers represent N value for each group. Asterisk indicates temperature at which recovery ratio was different from unity (P=0.04). Discussion Effect of accl imation period Ucr i t is a complex phenotype determined by the biochemistry and physiology of the muscular, cardiovascular, and respiratory systems. Sub-optimal function of these systems is known to occur on either side of species-specific temperature preferenda (Fry 1947; Farrell 2002; Lee et al. 2003a) and is likely to negatively impact swimming performance (Bennett 1990). Consequently, a fish's ability to hunt, evade predators, complete migrations and reproduce successfully may be jeopardized when temperatures are outside optimal ranges and swimming capacity is compromised. The ability to cope with extreme or variable thermal environments is therefore essential to the survival and fitness of fishes. Dealing with frequent and large temperature 29 changes is particularly important to fish like cutthroat trout. This species occupies a range of habitats from small streams to large rivers, representing an array of diverse thermal environments. In addition to seasonal flux of more than 20° C , cutthroat trout in some systems encounter diel fluctuations of 1 0 - 1 3 ° C (Schrank et al. 2003). Cutthroat trout subjected to temperature changes as great as + 8 ° C performed equally well on repeat U c r i t tests conducted after 48 h acclimation as they did after 3 weeks acclimation to that temperature. We contend that cutthroat trout can compensate sufficiently at the molecular, cellular and systems level within 48 h to offset any detrimental effects of acute temperature change on the performance of repeat U c r i t tests. Because recovery ratio was not affected by the short acclimation period we suggest that processes underlying metabolic recovery from exhaustive exercise were also similarly adjusted. Given their thermal ecology, this ability to acclimate rapidly to prevent impairment of swimming capacity could be of particular importance to cutthroat trout. Our results also indicate that a thermal acclimation period of 48 h should be acceptable when examining the effects of temperature on the swimming performance of cutthroat trout, and potentially other salmonids. Effect of temperature on swimming performance For several salmonid species the relationship between swimming performance and temperature has been described as 'bell-shaped' with a clear optimal temperature where U c r i t is maximal. This occurs at approximately 15° C for juvenile and adult sockeye salmon (O. nerka) (Brett 1964; Lee et al. 2003a), but it is important to note that fish are capable of very near-maximal performances at a range of several degrees around the defined optimum (Lee et al. 2003a). Similar plateaus where U c r i t is temperature insensitive occur between 5 -15° C in diploid brown trout (Salmo trutta) (Beaumont et al. 1995; Day and Butler 1996), between 14 -18° C in triploid brown trout (Altamiras et al. 2002), between 1 4 - 1 7 ° C in rainbow trout (O. mykiss) (Randall and Brauner 1991), and between 5-11° C in adult coho salmon (Lee et al. 2003a). Conversely, U c r i t for juvenile coho salmon (O. kisutch) has been shown to increase steadily with temperature to 2 0 ° C , and decline at higher temperatures (Glova and Mclnerney 1977). As per Fry's paradigm (1947) these optimal ranges generally reflect both the species' final temperature preferendum and most common thermal conditions of its field distribution. 30 In these cutthroat trout, both U c r , t_i and U c r j t -2 increased with temperature, although the temperature effect only approached statistical significance for U c r i t -2 - Therefore the similarity of swimming performance for the two acclimation periods cannot be ascribed to lack of a temperature effect on swimming performance. Furthermore, the optimal temperature for swimming performance appears to lie at or above 18 .0° C, the highest temperature tested here. This is quite likely as cutthroat trout tolerate temperatures up to 30° C (Heath 1963) and often encounter waters as warm as 2 7 ° C in summer months (Schrank et al. 2003). Other Pacific salmonids rarely encounter such warm water and this is reflected in somewhat lower critical thermal maxima in sockeye salmon (25° C), coho salmon (25° C) and rainbow trout (27e C) (Houston 1982). Effect of temperature on recovery ratio The ability to recover from exhaustive exercise to repeat a swimming challenge is of ecological relevance to many salmonids (Jain et al. 1998). Recovery involves the restoration of muscle glycogen, phosphocreatine (PCr) and adenosine triphosphate (ATP) stores and the clearance of lactate and other metabolites (Milligan 1996). Time required to recover reflects both the magnitude of the metabolic disturbance that must be corrected, and the speed at which these recovery processes can occur. Most studies have reported that full metabolic recovery from exhaustive exercise requires 8-24 hours. It has been demonstrated, however, that several salmonid species can perform equally well on repeat U c r j t tests that are separated by recovery periods far too brief (40 minutes to 2 hours) to facilitate complete metabolic recovery (Brauner et al. 1994; Farrell et al. 1998; Jain et al. 1998; Tierney 2000; Lee 2002). In such cases, metabolic recovery undoubtedly continues into the early stages of the subsequent swim trial, though not likely to completion. This suggests that some species are capable of swimming maximally while in a state of metabolic disturbance, and that some recovery processes can likely be postponed until the second swimming challenge is completed (Farrell et al. 2003). In the present experiment, individual recovery ratios were quite variable, preventing all but the 14° C group from testing significantly different from unity. On average, however, these hatchery-reared cutthroat trout were not as capable as recovering between consecutive U c r i t tests as wild salmon (Lee 2002; Farrell et al. 2003) and hatchery-reared rainbow trout (Jain et al. 1998). The rearing environment of these cultured cutthroat trout may have contributed to a 31 diminished ability to recover and re-perform U c r i t tests. This is consistent with the report by Brauner et al. (1994), that hatchery coho salmon exhibited lower recovery ratios than wild coho tested under the same conditions. Alternatively, perhaps cutthroat trout use more anaerobic swimming than other salmonids and need a longer recovery period to repeat their initial, relatively high U c r it- i performance. It is possible that these hatchery cutthroat trout would have been able to repeat critical swimming speeds given a slightly longer recovery period (~ 1 hour) between tests. We found no detectable effect of acclimation temperature on recovery ratio in cutthroat trout. Previous studies have noted that the recovery ratio decreased from unity at high temperatures in rainbow trout (Jain 1999) and in female sockeye salmon (Tierney 2000). In rainbow trout, the decrease in recovery ratio was positively correlated to U c r i t - i . which increased with experimental temperature. Presumably the larger metabolic disturbances created at faster swimming speeds could not be corrected in the allotted recovery period, preventing warm, "fast" fish from repeating their exceptional performance in the second swim trial. No such correlation between recovery ratio and U c r i t- i existed here but perhaps experiments at temperatures greater than 18 °C would reveal a similar relationship for cutthroat trout. Conclusion Despite the clear dependence of U c r i t on water temperature, our results show that the phenotype of the cutthroat trout was sufficiently plastic that, for a given temperature, U c r i t was similar after either a brief (48 h) or a normal (3 weeks) acclimation period. This ability to rapidly compensate for temperature changes of several degrees and maintain swimming abilities could be of the utmost ecological importance and is potentially adaptive for salmonids that occupy thermally variable environments. This information will benefit researchers who are time-constrained by logistics and those who choose to minimize laboratory acclimation in favour of studying fish that are as close as possible to their field-acclimatized state. Acknowledgements This research was funded by the Natural Sciences and Engineering Research Council of Canada (NSERC). Personal support was provided by an N S E R C post-graduate scholarship to M J M . Logistical support was provided by Fisheries and Oceans Canada. Thanks to Colin Brauner for 32 input on experimental design. Special thanks to Dale Larsen and the Fraser Valley Trout Hatchery for supplying fish and to the staff at the Cultus Lake Laboratory, particularly Bryan Smith. Assistance from Andrew Lotto and Chris Lee was greatly appreciated, as was input from Steven Cooke on an earlier version of the manuscript. 33 Literature cited Adams, S. R. and Parsons, G . R. (1998). Laboratory-based measurements of swimming performance and related metabolic rates of field-sampled smallmouth buffalo (Ictiobus bubalus): A study of seasonal changes. Physiological Zoology 71: 350-358. Albers, C , Manz, R., Muster, D. and Hughes, G . M . (1983). Effect of acclimation temperature on oxygen transport in the blood of the carp, Cyprinus carpio. Respiration Physiology 52: 165-179. Altamiras, J . , Axelsson, M . , Claireaux, G . , Lefrancois, C , Mercier, C. and Farrell, A . P. (2002). Cardiorespiratory status of triploid brown trout during swimming at two acclimation temperatures. Journal of Fish Biology 60: 102-116. Beamish, F. W. H . (1964). Respiration of fishes with special emphasis on standard oxygen consumption II. Influence of weight and temperature on respiration of several species. Canadian Journal of Zoology 42: 177-188. Beaumont, M . W., Butler, P. J. and Taylor, E . W. (1995). Plasma ammonia concentration in brown trout in soft acidic water and its relationship to decreased swimming performance. Journal of Experimental Biology 198: 2213-2220. Beddow, T. A . , Leeuwen, J. L . v. and Johnston, I. A . (1995). Swimming kinematics of fast starts are altered by temperature acclimation in the marine fish Myoxocephalus scorpius. Bell, W. H . and Terhune, L . D. B. (1970). Water tunnel design for fisheries research. Technical Report. No. 195. Bennett, A . F. (1990). Thermal dependence of locomotor capacity. American Journal of Physiology 259: R253-R258. Brauner, C . J. , Iwama, G . K . and Randall, D. J. (1994). The effect of short-duration seawater exposure on the swimming performance of wild and hatchery-reared coho salmon (Onchorhynchus kisutch) during smoltification. Canadian Journal of Fisheries and Aquatic Science 51: 2188-2194. Brett, J. R. (1964). The respiratory metabolism and swimming performance of young sockeye salmon. Journal of the Fisheries Research Board of Canada 21: 1183-1226. Brett, J. R. (1971). Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon {Oncorhynchus nerka). American Zoologist 11: 99-113. Brett, J. R. and Glass, N . R. (1973). Metabolic rates and critical swimming speeds of sockeye salmon {Oncorhynchus nerka) in relation to size and temperature. Journal of the Fisheries Research Board of Canada 30: 379-387. Burgetz, I. J . , Rojas-Vargas, A . , Hinch, S. G . and Randall, D. J. (1998). Initial recruitment of anaerobic metabolism during sub-maximal swimming in rainbow trout (Oncorhynchus mykiss). Journal of Experimental Biology 201: 2711-2721. 34 Burns, J. R. (1975). Seasonal changes in the respiration of pumpkinseed, Lepomis gibbosus, correlated with temperature, day length, and stage of reproductive development. Physiological Zoology 48: 142-149. Claireaux, G . , Webber, D. M . , Lagadere, J.-P. and Kerr, S. R. (2000). Influence of water temperature and oxygenation on the aerobic metabolic scope of Atlantic cod (Gadus morhua). Journal of Sea Research 44: 257-265. Cooke, S. J. , Grant, E . C , Schreer, J. F., Philipp, D. P. and Devries, A . L . (2003). Low temperature cardiac response to exhaustive exercise in fish with different levels of winter quiescence. Comparitive Biochemistry and Physiology 134A: 157-165. Day, N . and Butler, P. J. (1996). Environmental acidity and white muscle recruitment during swimming in the brown trout (Salmo truttd). Journal of Experimental Biology 199: 1947-1959. Farrell, A . P. (2002). Cardiorespiratory performance in salmonids during exercise at high temperature: insights into cardiovascular design limitations in fishes. Comparitive Biochemistry and Physiology 132A: 797-810. Farrell, A . P., Gamperl, A . K . and Birtwell, I. K . (1998). Prolonged swimming, recovery and repeat swimming performance of mature sockeye salmon Oncorhynchus nerka exposed to moderate hypoxia and pentachlorophenol. Journal of Experimental Biology 201: 2183-2193. Farrell, A . P., Gamperl, A . K . , Hicks, J. M . T. , Shiels, H . A . and Jain, K . E . (1996). Maximum cardiac performance of rainbow trout (Oncorhynchus mykiss) at temperatures approaching their upper lethal limit. Journal of Experimental Biology 199: 663-672. Farrell, A . P., Lee, C . G . , Tierney, K. , Hodaly, A . , Clutterham, S., Healey, M . C , Hinch, S. G . and Lotto, A . (2003). Field-based measurements of oxygen uptake and swimming performance with adult Pacific salmon using a mobile respirometer swim tunnel. Journal of Fish Biology 62: 64-84. Franklin, C . E . (1998). Studies of evolutionary temperature adaptation: muscle function and locomotor performance in Antarctic fish. Clinical and Experimental Pharmacology and Physiology 25: 753-756. Fry, F. E . J. (1947). Effects of the environment on animal activity. University of Toronto Studies, Biological Series 55: 1-62. Fry, F. E . J. and Hart, J. S. (1948a). The relation of temperature to oxygen consumption in the goldfish. Biological Bulletin 94: 66-77. Fry, F. E . J. and Hart, J. S. (1948b). Cruising speed of goldfish in relation to water temperature. Journal of the Fisheries Research Board of Canada 7: 169-175. Fuiman, L . A . and Batty, R. S. (1997). What a drag it is getting cold: partitioning the physical and physiological effects of temperature on fish swimming. Journal of Experimental Biology 200: 1745-1755. 35 Glova, G . J. and Mclnerney, J. E . (1977). Critical swimming speeds of coho salmon (Oncorhynchus keta) fry to smolt stages in relation to salinity and temperature. Journal of the Fisheries Research Board of Canada 34: 151-154. Griffiths, J. S. and Alderdice, D. F. (1972). Effects of acclimation and acute temperature experience on the swimming speed of juvenile coho salmon. Journal of the Fisheries Research Board of Canada 29: 251-264. Guderley, H . , Leroy, P. H . and Gagne, A . (2001). Thermal acclimation, growth and burst swimming ability of threespine stickleback: enzymatic correlates and influence of photoperiod. Physiological and Biochemical Zoology 74: 66-74. Hammer, C. (1995). Fatigue and exercise tests with fish. Comparitive Biochemistry and Physiology 112A: 1-20. Heath, W . G . (1963). Thermoperiodism in the sea-run cutthroat trout (Salmo clarkii clarkii). Science 142: 486-488. Houston, A . H . (1982). Thermal effects upon fishes. Publication of the Environmental Secretariat. No. 18566. Idler, D. R. and Clemens, W. A . (1959). The energy expenditures of Fraser River sockeye salmon during the spawning migration to Chilko and Stuart lakes. Progress Report. No. 6. Jain, K. E . (1999). Recovery of swimming performance in rainbow trout, its relationship to metabolic status and the effect of Cortisol blockade. M.Sc. thesis, Simon Fraser University, Burnaby, British Columbia. Jain, K . E . , Hamilton, J. C . and Farrell, A . P. (1997). Use of a ramp velocity test to measure critical swimming speed in rainbow trout. Comparitive Biochemical Physiology 117A: 441-444. Jain, K . E . , Birtwell, I. K . and Farrell, A . P. (1998). Repeat swimming performance of mature sockeye salmon following a brief recovery period: a proposed measure of fish health and water quality. Canadian Journal of Zoology 76: 1488-1496. Johnston, I. A . and Dunn, J. (1987). Temperature acclimation and metabolism in ectotherms with particular reference to teleost fish. In Temperature in Animal Cells. Edited by B. J. Fuller. Society for Experimental Biology, Great Britain, pp. 67-93. Keen, J. E . and Farrell, A . P. (1994). Maximum prolonged swimming speed and maximum cardiac performance of rainbow trout, Oncorhynchus mykiss, acclimated to two different water temperatures. Comparitive Biochemistry and Physiology 108A: 287-295. Kolok, A . S. and Farrell, A . P. (1994a). Individual variation in the swimming performance and cardiac performance of Northern Squawfish, Ptychocheilus oregonensis. Physiological Zoology 67: 706-722. Kolok, A . S. and Farrell, A . P. (1994b). The relationship between maximum cardiac output and swimming performance in northern squawfish, Ptychocheilus oregonensis: the effect of coronary artery ligation. Canadian Journal of Zoology 72: 1687-1690. 36 Lee, C . G . , Farrell, A . P., Lotto, A . , MacNutt, M . J. , Hinch, S. G . and Healey, M . C . (2003a). The effect of temperature on swimming performance and oxygen uptake in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks. Journal of Experimental Biology. 206: 3239-3251. Lee, C . G . , Farrell, A . P., Lotto, A . , Hinch, S. G . and Healey, M . C . (2003b). Excess post-exercise oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks following critical speed swimming. Journal of Experimental Biology 206: 3253-3260. Milligan, C . L . (1996). Metabolic recovery from exhaustive exercise in rainbow trout. Comparitive Biochemistry and Physiology 113A: 51-60. Mochan, D. G . and Mrazik, S. (2000). A summary of chemistry, temperature, habitat and macroinvertebrate data from the Southeast Oregon ambient monitoring sites (1992-1998). Technical Report. BIO00-03. Peterson, R. H . and Anderson, J. M . (1969). Influence of temperature change on spontaneous locomotor activity and oxygen consumption of Atlantic salmon , Salmo salar, acclimated to two temperatures. Journal of the Fisheries Research Board of Canada 26: 93-109. Randall, D. J. and Brauner, C. (1991). Effects of environmental factors on exercise in fish. Journal of Experimental Biology 160: 113-126. Rome, L . C , Funke, R. P. and Alexander, R. M . (1990). The influence of temperature on muscle velocity and sustained performance in swimming carp. Journal of Experimental Biology 154: 163-178. Schrank, A . J. , Rahel, F. J. and Johnstone, H . C. (2003). Evaluating laboratory-derived thermal criteria in the field: an example involving Bonneville cutthroat trout. Transactions of the American Fisheries Society 132: 100-109. Tierney, K . (2000). The repeated swimming performance of sockeye, coho and rainbow trout in varying conditions. M.Sc. thesis,Simon Fraser University, Burnaby, B . C . Venables, B. J. , Pearson, W. D. and Fitzpatrick, L . C. (1977). Thermal and metabolic relations of largemouth bass, Micropterus salmoides, from a heated reservoir and a hatchery in North Central Texas. Comparitive Biochemistry and Physiology 57A: 93-98. Williams, I. V . , Brett, J. R., Bell, G . R., Traxler, G . S., Bagshaw, J. , McBride, J. R., Fagerlund, U . H . M . , Dye, H . M . , Sumpter, J. P., Donaldson, E . M . , Bilinski, E . , Tsuyuki, H . , Peters, M . D., Choromanski, E . M . , Cheng, J. H . Y . and Coleridge, W. L . (1986). The 1983 early run Fraser and Thompson River pink salmon; morphology, energetics and fish health. Bulletin. XXIII. 37 Chapter 3. Effects of temperature on swimming performance, energetics and aerobic capacities of adult migrating pink salmon (Oncorhynchus gorbuscha): a comparison with sockeye salmon (O. nerka) Abstract The ability of individuals to successfully complete the spawning migration within a fixed energy budget and with changing river temperatures is critical to the continuance of Pacific salmon populations. While swimming energetics have been well documented for sockeye salmon (Oncorhynchus nerka), similar knowledge for pink salmon (O. gorbuscha) is primarily anecdotal. We assessed the prolonged swimming performance (U.n i), minimum and maximum metabolic rate (Mo, m m and M o , n m ) , and oxygen cost of transport (COT) for upper Fraser River pink salmon and compared them with those for sockeye salmon across a range of naturally occurring river temperatures using two large Brett-type swim tunnel respirometers. Contrary to previous beliefs, pink salmon were capable of similar relative critical swimming speeds (U . J as sockeye salmon (2.25 FL-s"'), but sockeye salmon swam to a higher absolute U n l (125.9 cm-s'1) than pink salmon (116.4 cm-s') because of their larger size (fork length = mean ± S E M ; sockeye salmon: 59.3 ± 0.8 cm; pink salmon: 53.5 ± 0.7 cm). However, some individual pink salmon swam faster than all individual sockeye salmon. Metabolic rate increased exponentially with swimming speed (P < 0.01) in both species and was higher for pink than sockeye salmon (P = 0.01), but swimming efficiency (cost of transport; COT) was not different between the species at their optimal swimming speeds. The upper and lower limits of metabolism also increased exponentially with temperature (Mo, m m P = 0.01; M o , n m , P < 0.01, respectively) but were not different between species ( M o 2 m m P = 0.93; M o w , P = 0.38). The relationship between Mo, and swimming speed was positively affected by temperature in pink salmon (P = 0.01), but average and minimum C O T s were independent of temperature in both species. Overall, a higher degree of inter-individual variability in pink salmon suggest that this species might not be as locally adapted to particular upriver migrations as are sockeye salmon. 38 Introduction Pink salmon [Oncorhynchus gorbuscha) and sockeye salmon (O. nerka) are the two most abundant of the Pacific salmon species and the sustainability of healthy stocks is of great interest to scientists, managers and fishers. Sockeye salmon have been studied extensively and their swimming performance, energetics and migration behaviour have been well documented. However, very little is known about swimming performance and energy use in adult migrating pink salmon. Several important differences between the life histories of these two anadromous, semelparous species are known. Pink salmon fry migrate to sea immediately upon emergence from the gravel and mature at sea for only eighteen months before returning to natal streams to spawn (Heard 1991). Sockeye salmon rear in lakes for one to three years before migrating seaward and one to four more years are spent maturing in the ocean before fish return to spawn at a minimum of age four (Burgner 1991). However, pink salmon grow much more quickly and their size at maturity is only slightly smaller than that of sockeye salmon (2.61 versus 2.73 kg in the Fraser River) (Burgner 1991; Heard 1991). Sockeye salmon tend to undertake relatively long upriver migrations and are assumed to be the strongest, and most efficient swimmers of all the Fraser River salmon (Burgner 1991). Pink salmon are capable of spawning within kilometres of the ocean and generally undertake much shorter, less difficult migrations. For this reason, pink salmon are considered the weakest swimmers of all the Pacific salmon (Heard, 1991). Recent increases in en route and pre-spawning mortality in many Fraser River salmon stocks have emphasized the potential impact of adverse river conditions on the successful completion of the spawning migration (Macdonald 2000; Macdonald et al. 2000; Lapointe 2002). Of particular concern are the potential impacts of increasing river temperatures. Climate models have predicted a 2-4 °C increase in air temperatures throughout British Columbia over the next 50-100 years (Boer 1992). In turn, mean summer water temperature in the Fraser River is predicted to rise 1.9 °C by 2099 with the largest increase (3.5 °C) occurring in mid July (Morrison et al. 2001) when early migrating sockeye salmon are en route to spawning grounds. Apart from climate change, encountered river temperatures can change several degrees throughout the duration of an individual's spawning migration, particularly for sockeye migrating long distances upriver. For example, early Stuart and Horsefly sockeye salmon enter the Fraser River in July when water temperature is around 15 ° C . Temperatures increase throughout their migrations to a 39 maximum of 22 °C before cooling rapidly at the spawning grounds. Chilko sockeye salmon migrate slightly later in the summer when the Fraser River approaches 17 - 2 0 ° C , but enter the cooler (14 °C) Chilcotin and Chilko Rivers for the final 200 km of their 624 km migration (Gilhousen 1990; Macdonald et al. 2000). Upper Fraser River pink salmon begin their migrations in September when river temperature has cooled slightly, and due to their shorter migration distance encounter a narrower range of river temperatures (13-16 °C) . The effects of temperature on the swimming performance and metabolism of salmonids have been examined extensively. Above an optimum, temperature is detrimental to swimming ability (Bennett 1990) and warmer water increases the energetic costs of swimming (Fry 1971). The latter is of particular importance to Pacific salmon migrating up-river to spawn. Upon entering freshwater, these fish stop feeding and therefore rely solely on stored body energy to complete the energetically expensive migration, sexual maturation, and spawning behaviours (Brett 1995). Inefficient migration or increased costs imposed by high temperatures can lead to inappropriate allocation of body energy reserves. This limits the amount of energy available for reproductive development, and may ultimately compromise the quality and viability of gametes. We compared the critical swimming performance (U c r i t) and energy use of upper Fraser River pink salmon and early Stuart sockeye salmon across a range of naturally occurring temperatures. These fish were chosen for the interspecific comparison because they represent the longest distance migrants, and therefore likely the highest performing stocks, of each respective species. Though comparisons were never direct, previous studies on the swimming performance and energetics of pink salmon suggest that pink salmon are capable of similar (Williams et al. 1986) or lower (Brett 1982; Milliken 1983) critical swimming speeds than sockeye salmon, and tend to have higher metabolic rates (i.e. were less energetically efficient than sockeye salmon) (Milliken 1983; Williams et al. 1986). We predicted that when compared directly, sockeye salmon would be capable of higher critical swimming speeds and perhaps more energetically efficient than pink salmon. Evidence suggests that selection imposed by the difficulty (distance and elevation) of upriver migration has resulted in divergent evolution of swimming performance and energetics in stocks of Fraser River sockeye salmon (Crossin 2002; Lee et al. 2003a) and it might also be expected that salmon stocks have evolved in response to temperature experiences during their spawning migration. Therefore we also expected that U c r j , and metabolic parameters would be more temperature-sensitive in pink salmon that are accustomed to a narrow range of river 40 temperatures than in sockeye salmon that encounter a broad range of temperatures during their spawning migration. Materials and methods Study animals Twelve early Stuart sockeye salmon (upriver migration distance = 1089 km, elevation = 701 m) and 53 upper Fraser River (Seton/Thompson) pink salmon (323 km; 401 m) were collected from the Fraser River and its tributaries (Figure 3.1) during upriver spawning migration between July and September 2001. Fish were caught with knotless cotton dip nets and were transported to the Fisheries and Oceans Canada laboratory in Cultus Lake, B C in a 330 L insulated transport tank. Transport water was chilled with block ice and contained a dilute Marinil anaesthetic (0.02 mg-L" 1 metomidate hydrochloride, Syndel International Inc., Vancouver, BC) to calm the fish. Compressed air was bubbled into the tank through an air stone to maintain water oxygen concentration above 7 mg 02 - L"\ No more than ten fish were transported at a time. Al l the sockeye salmon, and half the pink salmon were collected from Hell's Gate Fishway, approximately 200 km from Cultus Lake. The remaining pink salmon were collected from the fish ladder at the B C Hydroelectric Dam in Lillooett, B C , 450 km from Cultus Lake. The latter pink salmon were undoubtedly spawning in the Seton River, however those collected at Hell's Gate could have been migrating to either Seton or Thompson River. Upon arrival at the Cultus Lake Lab, fish were transferred to 1200 L holding tanks (maximum six fish per tank) at ambient river temperature for a 24-hour recovery period. To prepare for testing at temperatures throughout the range of ambient ± 5° C , some fish were moved to warmer or cooler temperatures at a rate of 1-2° C-day"1. Because a closely related species, the cutthroat trout (O. clarki clarki), was capable of withstanding much more rapid change (1° C-hour"1), this was considered an acceptable rate of temperature change in terms of the assessments of swimming performance made here (see Chapter 2). The evening prior to swim testing, and after a minimum of 48 hours and up to 5 days of thermal acclimation, a fish was transferred to a 40 L tub and lightly anaesthetized in buffered 0.2 mg-L"1 41 60 N 120W - 114 W Figure 3.1 Map of British Columbia, Canada showing the Fraser River watershed, including sampling locations (star: Hell's Gate; Y: Yale, B: BC Hydroelectric Dam), testing sites (C: Cultus Lake, B: BC Hydroelectric Dam, S: Simon Fraser University) and potential spawning grounds of upper Fraser River pink salmon (solid circle: Seton River; solid oval: Thompson River) and early Stuart sockeye salmon (broken oval). MS-222 (tricaine methoanosulfonate, Syndel International Inc., Vancouver, BC). Body mass (kg), fork length (FL; cm), maximum depth (d; cm) and width (w; cm) were measured before introducing the fish to the respirometer. The fish habituated to the tunnel for approximately one hour at a water velocity of 0.45 FL-s"1 and then performed a conditioning swim test (pink salmon only). This entailed increasing the water velocity by 0.15 FL-s*1 increments every two minutes until the fish 'failed', or was no longer able to swim against the current. Upon failure, the water velocity was returned to 0.45 FL-s"1 to allow an overnight recovery and habituation of 12-16 42 hours. Water at experimental temperature was continuously delivered to the respirometer to ensure sufficient dissolved oxygen concentration (> 7 mg CVL" 1 ) . Following swim testing, the fish was removed from the respirometer and killed by a blow to the head. Internal visual inspections were performed, fish were sexed, and the gonads removed and weighed to determine the gonadosomatic index (GSI = gonad mass / total mass x 100). Evaluat ing swimming performance Two mobile Brett-type swim tunnels (471.2 L , internal diameter of swimming chamber (ID)=25.4 cm; and 287.4 L , ID=20.3 cm) were used to conduct swimming tests (Farrell et al. 2003), which allowed two fish to be tested each day. (For more information on swim tunnels see www.sfu.ca/biology/facultv/swimtunnel/swimtunnel.html.) The swimming test consisted of a modified repeat ramp-U c r i t test as described by Jain et al. (1997). Fish were ramped up to 50-70% of the maximum speed attained in the conditioning test (51-100% of U c r i t ) using increments of 0.15 FL-s"1 at five-minute intervals. Thereafter, water velocity was increased by 0.15 FL-s"1 every 20 minutes until the fish failed. The fish was then allowed to recover at 0.45 F L - s - 1 for 45 minutes before performing a second ramp-Ucrit test. U c r j t values (FL-s"1) were calculated as in Brett (1964): Ucrit =Uf+ (tj/tixUi) where U f is the water velocity of the last fully completed interval (FL-s"1); tf is amount of time spent in the failed interval (min); ti is the length of each interval (20 min); and U i is the velocity increment (0.15 FL-s"1). Calculations were considered valid only if the fish completed at least two twenty-minute intervals before failure. U c r i t values were adjusted for the error due to solid blocking effects (Es) such that: Corrected Ucrit = Ucrit x (1 + Es) Es was calculated as described by Bell and Terhune (1970), assuming a streamlined shape factor: Es = 0.4x (FL/((w + d)/2)) x (AF/AT)L5 where F L is the fork length of the fish (cm); w and d are maximum body width and depth (cm); Ap is the cross sectional area of the fish (cm2); and A T is the cross sectional area of the tunnel (cm2). Assuming an elliptical shape, the cross sectional area of the fish was calculated as: 43 AF=n x((dxw)2/4) Evaluat ing energy use Dissolved oxygen concentration ([O2]) was measured using an OxyGuard Mark IV oxygen electrode (Point Four Systems, Delta, BC). Oxygen uptake was determined by removing air bubbles from the system and stopping water flow, then recording the decrease in [O2] over time. Oxygen consumption (M02; mg 02-kg"1-min~1) was calculated as: Mo2 = (A [OJ xV)/(mxt) where A[02] is the decrease in [O2] (mg O2); V is the volume of the respirometer (L; where V = total volume - mass of fish, assuming that 1 kg of fish occupies 1 L); m is the mass of the fish (kg); arid t is the time (min). Measurements were taken without a fish in the tunnel approximately twice each week, and indicated that background oxygen consumption was undetectable. M02 was measured while the fish was at rest prior to testing (one hour duration for pink salmon, ten minutes for sockeye salmon), throughout alternate five-minute velocity intervals, and for the last five to ten minutes of every twenty-minute velocity interval in both U c r i t trials, as well as for five minutes immediately prior to the second U r j t trial. Some measurement durations were slightly shorter if the water [O2] approached 7 mg 02 'L" 1 . Some fish were able to hold station without actively swimming up to the second speed interval (0.75 FL-s"1) and M02 measured during this period was sometimes lower than during the "routine" measurement period with water flow at 0.45 FL-s"1. This occurred five times, with an average reduction in routine metabolic rate of 9.6%. Occasionally, an individual's metabolic rate at the end of the U c r j t- i recovery period was also lower than its routine level. In order to most accurately estimate resting metabolic costs, we present the minimum-recorded M o 2 (Mo2-min) f ° r each individual. Conversely, although maximum oxygen uptake is generally considered to occur at U c r i t (Farrell and Steffensen 1987), in about 40% of fish M o 2 dropped off a very high swimming speeds, undoubtedly reflecting a metabolic shift to anaerobic pathways. In order to examine the upper limit of aerobic metabolism we therefore present the maximum-recorded M02 (Mo2-max) f ° r e a c n individual, whether from Trial 1 or 2. Aerobic metabolic scope was calculated as the difference between Mo2-m a x a n d Mo2-m i n. 44 It was determined that M02 at a given swimming speed was best predicted by fitting a four parameter sigmoidal curve to data obtained from each individual at intermediate swimming speeds. This modelled data was,used to calculate cost of transport (COT; mg 02 -kg"1-m~1) at each swimming speed such that: COT = Mo2/Ux 100/60 where M02 is the predicted oxygen consumption (mg 02-kg"1-min"1) at a given swimming speed, U (cm-s 1). The average value of C O T ( C O T a v e ) across all swimming speeds and the minimum calculated C O T ( C O T m i n ) were determined for each individual, as was the swimming speed at which C O T m i n occurred (UO P T). A n index of the state of recovery following the first swimming trial, i.e. 45 minutes post-U c ri t-i, was calculated as: 100 X (Mo2-Ucrit - Mo2-Ucrit+45)/(Mo2-Ucrit - Mo2-mJ where Mo 2-u Cr i t is the active metabolic rate measured at U c r i t - i , Mo2-ucrit+45 is the metabolic rate measured 45 minutes after failing the first U c r i t test, and Mo2-m i n is the lowest metabolic rate recorded for the individual throughout both U c r i t trials. Video analyses Al l swimming tests were recorded on time-lapse video to give a clear view of swimming movements from the ventral side. Tail beat frequencies (TBF; beats-min"1) were determined at every swimming speed for which there was oxygen consumption data. The swimming speed at which burst/coast behaviour began to consistently supplement steady body-caudal fin swimming was also determined by visual observation of the tail and body movements on the video. This speed of gait transition (UGT) was recorded as the swimming speed at which a fish was observed using burst/coast sequences (burst to the front of the tunnel followed by passive drifting to the rear of the tunnel), provided this behaviour continued throughout the remainder of the test. Data analyses and statistics To increase sample sizes and statistical power, two previously published data sets were included in analyses of U c r i t , recovery ratio, minimum and maximum M02, and aerobic scope. In 1999, seven Seton River pink salmon were dip-netted from the fish ladder at the B C Hydroelectrical 45 Dam (Lillooett, BC) and tested on-site following an overnight recovery (Farrell et al. 2003). In 2000, six early Stuart sockeye were dip-netted from the Fraser River, near Yale, B . C . (approximately 25 km downstream from Hell's Gate) and transported 150 km to Simon Fraser University where they were held a minimum of three days before swim testing (Lee et al. 2003a). In both studies tests were conducted in one of the Brett-type swim tunnels used in the present study and M02 sampling and U c r i t protocols were identical to those used on pink and sockeye salmon in 2001. Data from all fish tested in 1999, 2000 and 2001 were used in analyses of U c r i t and recovery ratio, Mo2-min and Mo2-max» and metabolic scope. Values for U c r i t were not calculated for three pink salmon (2001) that were too large for the swim tunnel (error due to solid blocking exceeded 25%). Two other pink salmon were unable to swim following the 45-minute recovery from the first U c r j t test. This did not seem to be related to performance on the first trial, as one fish attained 1.95 FL-s"1 in U c rit-i while the other fish was unable to swim even 1 FL-s" 1. Video and oxygen consumption data at intermediate speeds were available only for fish tested in 2001 (N = 10 sockeye salmon, 60.2 ± 0.87 cm F L , 2.52 ± 0.01 kg; N = 33 pink salmon, 53.7 ± 0.79 cm F L , 1.78 ± 0.01 kg). This subset of fish was used to examine aerobic costs of transport, and to carry out analyses of tail beat frequency and gait transition. Independent sample t-tests were used to compare fish length and weight between species and years, to compare recovery, C O T a v e and C O T m i n between species. Paired t-tests were used to compare C O T a v e and C O T m i n and the initial M02 recording between swimming trials. The effects of species (fixed factor), and temperature (covariate) on recovery ratio, C O T a v e , C O T m j n and log-transformed Mo2-mim Mo2-max a r | d metabolic scope were examined using analysis of covariance ( A N C O V A ) . When the effect of species and interaction terms were not significant, pink and sockeye salmon data were pooled and G L M regression was used to examine the effects of temperature. If a species effect was evident, the effect of temperature was examined on pink and sockeye salmon independently. Similarly, effects on log-transformed swim speed-Mo2, swim speed-TBF and M02-TBF relationships were examined using A N C O V A and regression with repeated measures. These repeated measures tests were conducted using R statistical software (Version 1.6.2, R Development Core Team) and all other analyses were carried out using SPSS 10.0 statistical package (SPSS Science, Chicago, Illinois). Differences were considered significant when P<0.05. 46 Results Overall, sockeye salmon that performed swimming tests (N = 16, mean ± S E M = 59.3 ± 0.84 cm F L , 2.33 ± 0.10 kg) were significantly longer (P < 0.01) and heavier (P < 0.01) than pink salmon that were tested (N = 40, 53.5 ± 0.67 cm F L , 1.78 ± 0 . 0 1 kg) but there were no significant between-year differences within species for fish size (pink P = 0.56, sockeye P = 0.18). Swimming performance Performance was not consistently better on either the first or second U c r i t trial (Ucrit-i or U c r j t-2 respectively) but recovery ratios were generally scattered on either side of unity throughout the range of temperatures tested (mean ± SEM = 1.01 ± 0.02; range = 0.5 to 1.75). Because U c r j t is meant to measure the maximum speed that can be maintained for a given time we present the higher of the two U c r j t values for each fish (U c r i t . m a x ; Figure 3.2). Ucrit.max ranged from 1.25 to 3.15 FL-s"1 (mean ± S E M = 2.25 ± 0.06 FL-s"1). Both species were capable of similar critical swimming speeds in FL-s"1 (sockeye salmon: 2.26 ± 0.08 FL-s" 1; pink salmon: 2.25 ± 0.08 FL-s"1) Figure 3.2A) but limited overlap of the 95% confidence intervals in Figure 3.2B indicates that sockeye salmon can generally swim at faster absolute speeds (129.6 ± 4.0 cm-s"1) than pink salmon (118.4 ± 4.4 cm-s"1). However, some individual pink salmon swam faster than all individual sockeye salmon. Pink salmon displayed their first burst-coast sequence at a range of 71-100% of U c r i l (mean ± S E M = 89.1 ± 2.1 %; N=20). This was not significantly different from sockeye salmon (t-test; P = 0.36; N=9), which initiated bursting behaviour at 86-100 % of U c r i t (93.6 + 2.8 %). Approximately half of all individuals eventually exhibited the burst-coast sequence at least three times per minute. In most cases this occurred only throughout the last five minutes of the test, but in three pink salmon the behaviour persisted for more than 70 minutes. One sockeye salmon (U c r i l l = 1.88 FL-s'1) and one pink salmon (U c r i l , = 1.95 FL-s"1) completed the first swimming trial without exhibiting any bursting behaviour. These U c r i l , values were lower than their respective species' averages though the difference was significant only for the sockeye salmon individual (t-test; P = 0.02). 47 Figure 3.2. Maximum critical swimming speed for pink (o, —) and sockeye salmon (•, —) in (A) FL-s 1 and (B) cm-s"1. The quadratic curve of best fit is shown for each species with 95% confidence intervals. Metabol ic parameters Both Mo2-min ar>d Mo2-max (Figure 3.3A) increased exponentially with temperature ( A N C O V A ; P = 0.01 and P < 0.01 respectively) but neither relationship was different between species ( A N C O V A ; P = 0.93; P = 0.38) nor showed an interaction between species and temperature ( A N C O V A ; P = 0.94; P = 0.53). A N C O V A revealed that aerobic metabolic scope (Figure 3.3B) 25 n O 0 -I ^ , . 1 1 , 1 , 0 8 10 12 14 16 18 20 22 Temperature (°C) Figure 3.3. (A) Minimum (o pink salmon; • sockeye salmon) and maximum (• pink salmon; • sockeye salmon) rates of oxygen consumption of fish performing repeat U c r i t tests at a range of naturally occurring temperatures and (B) the resulting aerobic metabolic scope (Scope = Mo 2 .ma X - Mo 2 -mi n ; ° pink salmon; • sockeye salmon). 49 was not different between aerobic metabolic scope (Figure 3.3B) was not different between species (P = 0.50) and when data were pooled for both species scope was not affected by temperature (P = 0.09). However, the lack of a temperature effect was primarily due to the large variability among pink salmon and there was a statistically significant relationship between metabolic scope and temperature when sockeye salmon were considered separately ( G L M ; P < 0.01). Recovery from exhaustive exercise Fish recovered sufficiently well after swimming to exhaustion in U c rj t-i that recovery ratio (U c rj t-2/Ucrit-i) was not significantly different from unity for either pink salmon (mean ± S E M = 1 .02±0 .04; t-test, P = 0.53) or sockeye salmon (RR=0.99 ± 0.03; t-test, P = 0.76). A N C O V A revealed no effect of species (P = 0.94), temperature (P = 0.18) or an interaction of main effects (P = 1.00) on recovery ratio. When data were pooled for both species, recovery ratio did not show a significant relationship with temperature ( G L M ; P = 0.09). Within 45 minutes after the first U c r i , trial, pink salmon M02 had recovered from 35 to 99% toward resting level, while sockeye salmon had recovered 57 to 100%. Though these ranges were similar, on average sockeye salmon were closer to completely restoring resting metabolic rate (mean + S E M = 85 ± 5%) than were pink salmon (71 ± 4%; t-test P=0.04). Fish from both species that had not recovered completely exhibited slightly elevated metabolic rates into the early stages of Trial 2 but by the second swimming interval, M02 was no higher than previously measured in Trial 1 (paired t-tests; sockeye salmon P = 0.21; pink salmon P = 0.28). However, in pink salmon the effect was sufficient that an interaction between swimming speed and trial was significant ( A N C O V A ; P = 0.05). There was no such interaction ( A N C O V A ; P = 0.94) or effect of trial ( A N C O V A ; P = 0.69) for sockeye salmon. Recovery ratio was not significantly related to the percent recovered from Ucrit-i in either pink ( G L M ; P = 0.27) or sockeye salmon ( G L M ; P = 0.49) Energetic costs of swimming The effect of species on the relationship between M02 and swimming speed was significant for both Trial 1 (Figure 3.4A; repeated measures A N C O V A ; P = 0.01) and Trial 2 (Figure 3.4B; repeated measures A N C O V A ; P < 0.01) with oxygen consumption consistently higher for pink 50 3 0 Figure 3.4. Rate of oxygen consumption at intermediate swimming speeds of Trial 1 (A) and Trial 2 (B) for pink (o) and sockeye salmon (•). salmon. Temperature was a significant covariate in this relationship for pink salmon (repeated measures A N C O V A ; Trial 1: P = 0.01; Trial 2: P = 0.02) but not for sockeye salmon (repeated measures A N C O V A ; Trial 1: P = 0.56; Trial 2: P = 0.22). There were sufficient data to individually model M02 versus swimming speed and calculate costs 51 of transport for 23 pink salmon and 9 sockeye salmon. Both C O T (Figure 3.5A) and C O T n e t (Figure 3.5B) were highly variable across swimming speeds for pink salmon. Costs of transport for sockeye salmon were more tightly clustered and overlapped with the lower half of pink salmon data. 180 Swimming speed (cm-s1) Figure 3.5. Costs of transport at intermediate swimming speeds for pink (N = 23) and sockeye salmon (N = 9). (A) Total cost of transport includes both the cost of swimming and the costs associated with standard or resting metabolism. (B) Net cost of transport excludes the resting metabolic rate and represents the energy spent only swimming. 52 Neither average nor minimum costs of transport (Table 3.1) were affected by temperature (ANCOVA; C O T a v e P = 0.69; C O T m i n P = 0.97), nor was the swimming speed at which C O T m i n occurred (ANCOVA; U o p t : P = 0.24). C O T a v e was higher for pink than sockeye salmon (t-test; P < 0.01) but there was no interspecific difference in COT m j n (t-test; P = 0.27) or U o p t (t-test; P =0.63). Based on the means of C O T a v e and COT m j n for each species, the energetic cost of the respective migrations was estimated (Table 3.1). Table 3.1. Estimated aerobic cost of swimming a distance equivalent to the entire upriver migration for upper Fraser River pink and early Stuart sockeye salmon. Calculations are based on the mean minimum and average costs of transport for each species. Pink salmon Sockeye salmon COT COT (mg Cost of 323 km COT COT Cost of 1089 km (mg 02kg' lm"1) 02-m"1) migration (MJ) (mg 02kg"1m"1) (mg 0 2m'') migration (MJ) Minimum 0.16 ±0.00 0.26 ± 0.02 1.14 ±0.10 0.14 + 0.01 0.34 ± 0.02 5.07 ±0.29 Average 0.23 ±0.01 0.36 ±0.02 1.58 ±0.10 0.17 ±0.01 0.42 ±0.02 6.19 ±0.31 Presented v alues are means ± SEM. The relationship between tail beat frequency and swimming speed (Figure 3.6A) was significantly different between pink and sockeye salmon (repeated measures A N C O V A ; P < 0.01). The oxygen cost of swimming with a given tail beat frequency was also different for pink and sockeye salmon, as indicated by the species-specific relationships between M02 and TBF (Figure 3.6B; repeated measures A N C O V A ; P < 0.01). Temperature affected only the relationship between M02-TBF for pink salmon (repeated measures A N C O V A ; P = 0.02). Discussion Swimming performance Anecdotal evidence, supported by some research, has suggested that pink salmon are inferior swimmers to sockeye salmon (Heard 1991). Brett (1982) found that sockeye outperformed pink salmon in 10 h prolonged swimming, at both relative (FL-s"1) and absolute (cm-s1) speeds. However, his comparisons are somewhat questionable as gravid female pink salmon tested at 202 C were compared to silver male and female sockeye salmon tested at 152 C. Conversely, 53 Figure 3.6. (A) Tail beat frequencies measured at intermediate swimming speeds for pink (o N = 20) and sockeye salmon (• N = 10). (B) Oxygen consumption rates associated with given tail beat frequencies. Williams and Brett (1987) measured the relative 30-minute U c r i t of adult pink salmon in the field to be comparable to those previously measured for sockeye. However, these results should also be considered carefully because U c r j t for each fish was adjusted to a common temperature of 15° using a formula developed for sockeye salmon. In the present study there were no between-54 species differences in the relative 20-minute Ucrit-max, D u t pink salmon did not reach the same absolute swimming speeds as sockeye salmon. Nonetheless, it is important to note that some individual pink salmon were capable of equal and higher critical swimming speeds than even the fastest sockeye salmon. The mean Ucrit-max of 2.25 FL-s" was similar to values previously recorded for adult sockeye salmon using similar protocols and equipment (Farrell et al. 2003: 1.81-2.25 B L - s 1 ; Lee et al. 2003a: 1.73-2.36 BL-s"1) as well as in unrelated studies (Brett 1965; Brett and Glass 1973). Williams and Brett (1987) measured U c r i t to be higher at 3.0 L-s"1 for upper Fraser river pink salmon but this difference may reflect the difficulty in comparing results of U c rit tests between studies using different protocols and equipment (Hammer 1995). Pink and sockeye salmon both supported steady state caudal fin swimming with burst-coast swimming at high speeds. Overall there were no major differences between species as to when bursting behaviour was initiated (89-93% of U c rj t). Both species were also able to swim to exhaustion and recover rapidly enough to repeat their first U c r i t performance. This ability has been previously demonstrated in both juvenile and adult Pacific salmon (Randall et al. 1987; Brauner et al. 1994; Jain et al. 1998; Tierney 2000; Lee et al. 2003a) but was not as evident in adult cutthroat trout (see Chapter 2). As with pink and sockeye salmon in this study, Lee et al. (2003b) recently reported that post-exercise metabolic rates in several stocks of sockeye and coho salmon (O. kisutch) returned to resting levels within approximately 45 minutes. This was accompanied by levels of excess post-exercise oxygen consumption that were much lower than reported for juvenile salmonids (Brett 1964; Scarabello et al. 1992), which may have reflected minimal anaerobic contribution to U c r i t swimming in these species. This is further supported by the limited use of burst-coast behaviour by most pink and sockeye salmon tested here, and may illustrate that pink and sockeye salmon are remarkably well adapted to performing repeated bouts of exhaustive exercise. Metabol ic parameters and cost of transport It has been shown repeatedly, and in different species, that U c r j t , resting and maximum oxygen consumption and metabolic scope all increase with warming to an optimum temperature, beyond which these variables begin to decrease (Fry and Hart 1948; Griffiths and Alderdice 1972; Rome et al. 1990; Keen and Farrell 1994; Claireaux et al. 2000). In this study, U c r i t showed a bell-shaped curve with an optimum around 16 °C for both pink and sockeye salmon. This is very similar to the reported optima of 15 °C for juvenile and adult sockeye salmon (Brett and Glass 55 1973) and 15-16 °C for two stocks of adult sockeye salmon (Lee et al. 2003a). However, as found by Lee et al. (2003a) peak swimming performance in both pink and sockeye salmon was possible across a relatively wide range of temperatures. Minimum and maximum metabolic rates increased exponentially with temperature and were not different between species. However, it should be pointed out that sockeye salmon data for M02-m a x almost always fell below the trend line fitted to data from both species. Considerable inter-individual variability among pink salmon concealed both a temperature and species effect on aerobic metabolic scope. However, when considering sockeye salmon alone, scope showed a strong positive relationship with increasing water temperature. There were no obvious decreases in any of these variables at higher temperatures. This may indicate an uncoupling of the optimal temperatures for swimming performance and metabolic scope, as has been shown previously in Fraser River sockeye salmon (Lee et al. 2003a). Although a limited number of sockeye salmon were tested at warmer temperatures and variability in pink salmon data was high, these results also cautiously suggest that temperatures of up to 20-22 °C may not be as detrimental to metabolic function as might have been expected. Mean values of COT m j n and C O T a v e for each species because of their potential usefulness in predicting actual costs of swimming upriver. C O T m i n occurs when an individual is swimming at its optimal speed and can be used to estimate the minimum energy required to swim a certain distance. However, during upriver migration, salmon swim at a range of speeds (Rand and Hinch 1998) and therefore C O T a v e may allow a more practical estimate of energy requirements. Support for our observed costs of transport is found in Lee (2002) who measured the aerobic COT for early Stuart sockeye swimming at U c rit as 0.17 mg 02,kg"1-m"1, the equivalent of our C O T a v e for the same stock of sockeye salmon. Swimming in a tunnel did prove to be more energetically expensive for pink than sockeye salmon, as demonstrated by upwards shift of the Mo2-swim speed curves and the higher COT a v e . This was a combined result of employing higher tail beat frequencies to attain a given swimming speed, and the increased oxygen cost of beating the tail at a given frequency. Williams et al. (1986) also found that pink salmon tend to have a 30% greater oxygen consumption at a given swimming speed than sockeye (Williams et al. 1986). However, body constituent analyses conducted in 1999 showed that Fraser River pink salmon tended to use slightly less absolute energy to complete their migration than Fraser River sockeye salmon that migrated similar distances (Crossin 2002). This discrepancy may be explained by 56 differences in migratory behaviour that are not evident when evaluating swimming energetics in a swim tunnel. E M G telemetry studies by Hinch et al (2002) suggested that pink salmon tend to swim closer to shore and cross the river less frequently than do sockeye salmon. Pink salmon also tended to swim more consistently near U c r i t , resulting in a lower coefficient of variation for swimming speed than sockeye salmon, which often burst to speeds well above U c r j t . One or both of these migration strategies may allow pink salmon to behaviourally compensate for their higher inherent metabolic rates and costs of swimming. There was no difference between species in C O T m i n , indicating that pink salmon are capable of swimming as efficiently as sockeye salmon, though over a restricted range of swimming speeds. By swimming at U o p t pink salmon could reduce total energy costs of the migration by 39%, compared to a reduction of 22% for sockeye salmon. Thus, pink salmon benefit from even greater energy savings than sockeye salmon by swimming at optimal speeds and this behaviour may be more strongly selected for in pink salmon. On average, we found that both species swam optimally at approximately 70 cm-s"1 but U o p t ranged from 50-90 crrrs"1 (0.75-1.6 FL-s"1) in sockeye salmon and from 32-130 cm-s 1 (0.6-2.5 FL-s"1) in pink salmon. E M G telemetry studies have shown that, in situ, pink and sockeye salmon migrate at mean swimming speeds of 2.21 and 1.60 BL-s"1 respectively (Hinch et al. 2002; Standen et al. 2002). However, these fish were observed while swimming through relatively challenging reaches in the Fraser canyon and may have foregone energy-saving behaviours such as swimming at optimal speeds in favour of minimizing migration time through these reaches (Hinch and Rand 2000; Standen et al. 2002). Conversely, sockeye salmon were observed swimming closer to predicted optimal speeds when encountering much slower river flows of -20 to 40 cm-s"1 (Hinch and Rand 2000). The above calculation of energy savings (taken from Table 3.1) is very crude and is intended only to give a rough comparison between the species. We are aware of three possible sources of error in the estimates. Firstly, the calculations do not include the cost of swimming against a current. Secondly, our calculations of C O T are entirely aerobic and do not consider the contribution of anaerobic metabolism to total swimming costs. Burgetz et al. (1998) demonstrated in rainbow trout (O. mykiss) that anaerobic pathways were being utilized at speeds of 70-80% of U c r i t and represented an additional oxygen cost of 76.9% of the measured oxygen consumption. More recently, Lee et al. (2003b) suggested that anaerobic metabolism may be initiated at as little as 60% of U c r i t in sockeye and coho salmon (O. kisutch) but that the total 57 contribution to oxygen costs were much less (only 1 1 - 3 4 % of the oxygen cost of an entire U C ri t test). Although the exact contribution has not been agreed upon, it is widely accepted that in situ, salmon regularly swim anaerobically and that the anaerobic contribution to bioenergetics models should be considered (Hinch et al. 1996; Rand and Hinch 1 9 9 8 ; Hinch et al. 2 0 0 2 ; Standen et al. 2 0 0 2 ; Hinch et al. 2 0 0 3 ) . Thirdly, we did not consider that Pacific salmon are able to adopt behaviours which allow them to exploit flow fields to gain forward-assists in river, thus reducing the energetic cost of migrating (Hinch and Rand 2 0 0 0 ; Standen 2 0 0 1 ) . This error acts in opposition to the previous one. Although it is well known that swimming costs increase in warmer water, the relationship between M02 and swimming speed was affected by temperature only in pink salmon. However, a small number of sockeye (N = 10) were spread across a temperature range of 11 .5 to 2 0 °C, such that a slight temperature effect might not have been detected. Interestingly though, neither C O T a v e nor C O T m j n were affected by temperature in either species. Thus even in pink salmon, swimming costs were not significantly increased in warmer water as expected. However, we suspect that the appropriate temperature effects might have been obscured by considerable inter-individual variability in swimming efficiency, particularly in pink salmon. One previous study of pink salmon swimming metabolism also noted "exceptionally wide scatter of points compared to data collected on sockeye" (Williams et al. 1986 ) . However metabolic rates that were elevated above baseline data were considered invalid and attributed to the excitable nature of some pink salmon. No evidence of such excitability in pink salmon behaviour was evident in this study either at the time of testing or upon review of the swimming videos. Potential relevance of inter-individual variability Of potentially equal ecological interest to the observed interspecific differences (or lack thereof) in the previous results are the consistent differences in intraspecific variation. The scatter in data points for swimming speed, Mo2-min, Mo2-max and metabolic scope are all much greater for pink than sockeye salmon across all temperatures. Even more obvious is the spread of total and net C O T for pink salmon as compared to sockeye salmon. In fact, measurements of U c r i t , Mo2-max, and C O T of what is considered a single stock-group of pink salmon more closely resembles the array of abilities exhibited by several stocks of sockeye salmon - from the relatively slow-swimming, energetically inefficient short distance migrating stocks, to the fast-swimming, 5 8 exceptionally efficient long distance migrating stocks (Lee et al. 2003a). Though variation in migratory behaviour may either compensate for or intensify the variation in swimming performance and energy efficiency within pink salmon, I suggest that the observed range may represent a mixed strategy of swimming physiologies within this species. Crossin (2002) noted that while sockeye salmon stocks showed a distinct gradient in energy stores and efficiency of energy use based on the difficulty of their migration, pink salmon from different spawning populations were remarkably similar in how they stored and used energy. In addition, higher straying rates (Heard 1991) and the genetic homogeneity of Fraser River pink salmon (Bruce White, Pacific Salmon Commission, Vancouver, B C , personal communication) suggest that pink salmon may not be as pre-programmed to return to natal streams to spawn but may actually be capable of altering their spawning destination depending on internal and external conditions during or prior to migration. The variability in swimming performance and efficiency of transport among individuals in this study also implies that pink salmon do not appear to be as locally adapted to particular spawning migrations as are sockeye salmon. Also, contrary to the prediction that pink salmon should be adapted to a narrower temperature range than sockeye salmon, individual pink salmon were capable of similar U c r i t s and costs of transport across the observed temperature range. Thus, in upper Fraser River pink salmon, some individuals exceed the minimal requirements of the generally rigid migration experience and might be capable of successfully migrating to more distant spawning grounds and encountering more variable temperature conditions. Conclusion Though effects of temperature on metabolism were notable, increasing temperature did not impair swimming abilities or increase the oxygen costs of swimming as markedly as was expected. The observed temperature-insensitivity of these parameters was especially surprising in pink salmon, given the relatively narrow temperature range encountered by this species during their spawning migration. Sockeye salmon swam to higher absolute critical swimming speeds than pink salmon and were slightly more energetically efficient. However, high variability within pink salmon resulted in some individuals that were equally fast and efficient swimmers as sockeye salmon. By maintaining such variation in swimming ability, energy efficiency, and temperature sensitivity among individuals, populations may be better able to cope with variable conditions or stochastic events. This may be of particular importance to pink salmon because 59 their two-year life span and strong dominance cycles make them vulnerable to extirpation following as little as one unsuccessful spawning season. Acknowledgements This research was funded by the Natural Sciences and Engineering Research Council of Canada (NSERC Strategic Grant to M H , A F and S H and N S E R C Research Grants to S H and A F . Personal support was provided by an N S E R C post-graduate scholarship to MJM.) Logistical and in-kind support was provided by Fisheries and Oceans Canada. We greatly appreciate the assistance of Yale First Nations in fish collection. Special thanks to the staff at the Cultus Lake Laboratory, particularly Bryan Smith and Dave Barnes. Field and lab assistance from Yuho Okada and Richard Anderson was greatly appreciated. Many thanks to Glenn Crossin for numerous discussions about energy use in pink and sockeye salmon. 6 0 Literature cited Bennett, A . F. (1990). Thermal dependence of locomotor capacity. American Journal of Physiology 259: R253-R258. Boer, G . J. , McFarlane, N . A . and Lazare, M . (1992). Greenhouse gas-induced climate change simulated with the C C C second-generation general circulation model. Journal of Climate 5: 1045-1077. Brauner, C. J. , Iwama, G . K . and Randall, D. J. (1994). The effect of short-duration seawater exposure on the swimming performance of wild and hatchery-reared coho salmon (Onchorhynchus kisutch) during smoltification. Canadian Journal of Fisheries and Aquatic Science 51: 2188-2194. Brett, J . R. (1964). The respiratory metabolism and swimming performance of young sockeye salmon. Journal of the Fisheries Research Board of Canada 21: 1183-1226. Brett, J. R. (1965). The relation of size to rate of oxygen consumption and sustained swimming speed of sockeye salmon {Oncorhynchus nerka). Journal of the Fisheries Research Board of Canada 22: 1491-1501. Brett, J. R. (1982). The swimming speed of adult pink salmon, Oncorhynchus gorbuscha, at 20C and a comparison with sockeye salmon, O. nerka. Canadian Technical Report of Fisheries and Aquatic Sciences. 1143. Brett, J . R. (1995). Energetics. In Physiological Ecology of Pacific Salmon. Edited by C . Groot, W. C . Clarke and L . Margolis. U B C Press, Vancouver, pp. 1-68. Brett, J. R. and Glass, N . R. (1973). Metabolic rates and critical swimming speeds of sockeye salmon (Oncorhynchus nerka) in relation to size and temperature. Journal of the Fisheries Research Board of Canada 30: 379-387. Burgetz, I. J. , Rojas-Vargas, A . , Hinch, S. G . and Randall, D. J. (1998). Initial recruitment of anaerobic metabolism during sub-maximal swimming in rainbow trout (Oncorhynchus mykiss). Journal of Experimental Biology 201: 2711-2721. Burgner, R. L . (1991). Life History of Sockeye Salmon (Oncorhyncus nerka). In Pacific Salmon Life Histories. Edited by C . Groot and L . Margolis. U B C Press, Vancouver, B C , Canada, pp. 3-117. Claireaux, G . , Webber, D. M . , Lagadere, J.-P. and Kerr, S. R. (2000). Influence of water temperature and oxygenation on the aerobic metabolic scope of Atlantic cod (Gadus morhua). Journal of Sea Research 44: 257-265. Crossin, G . T. (2002). Effects of ocean climate and upriver migratory constraints on the bioenergetics, fecundity, and morphology of wild, Fraser River salmon. M.Sc. thesis, University of British Columbia, Vancouver. Farrell, A . P. and Steffensen, J. F. (1987). A n analysis of the energetic costs of the branchial and cardiac pumps during sustained swimming. Fish Physiology and Biochemistry 4: 73-79. 61 Farrell, A . P., Lee, C. G . , Tierney, K. , Hodaly, A . , Clutterham, S., Healey, M . C . , Hinch, S. G . and Lotto, A . (2003). Field-based measurements of oxygen uptake and swimming performance with adult Pacific salmon using a mobile respirometer swim tunnel. Journal of Fish Biology 62: 64-84. Fry, F. E . J. (1971). The effects of environmental factors on the physiology of fish. In Fish Physiology. Edited by W. S. Hoar and D. J. Randall. Academic Press, New York. pp. 1-98. Fry, F. E . J. and Hart, J. S. (1948). Cruising speed of goldfish in relation to water temperature. Journal of Fisheries Research Board of Canada 7: 169-175. Gilhousen, P. (1990). Prespawning mortalities of sockeye salmon in the Fraser River system and possible causal factors. Bulletin. 22. Griffiths, J. S. and Alderdice, D. F. (1972). Effects of acclimation and acute temperature experience on the swimming speed of juvenile coho salmon. Journal of the Fisheries Research Board of Canada 29: 251-264. Hammer, C . (1995). Fatigue and exercise tests with fish. Comparitive Biochemistry and Physiology 112A: 1-20. Heard, W . R. (1991). Life History of Pink Salmon (Oncorhyncus gorbuscha). In Pacific Salmon Life Histories. Edited by C . Groot and L . Margolis. U B C Press, Vancouver, B C . pp. Hinch, S. G . and Rand, P. S. (2000). Optimal swimming speeds and forward-assisted propulsion: energy-conserving behaviours of upriver-migrating adult salmon. Canadian Journal of Fisheries and Aquatic Science 57: 2470-2478. Hinch, S. G . , Standen, E . M . , Healey, M . C . and Farrell, A . P. (2002). Swimming patterns and behaviour of upriver migrating adult pink {Oncorhynchus gorbuscha) and sockeye (O. nerka) salmon as assessed by E M G telemetry in the Fraser River, British Columbia, Canada. Hydrobiologia 483: 147-160. Hinch, S. G . , Standen, E . M . , Healey, M . C . and Farrell, A . P. (2003). Swimming patterns and behaviour of upriver migrating adult pink (Oncorhynchus gorbuscha) and sockeye (O. nerka) salmon as assessed by E M G telemetry in the Fraser River, British Columbia, Canada. Hydrobiologia Hinch, S. G. , Diewert, R. E . , Lissimore, T. J. , Prince, A . M . J. , Healey, M . C . and Henderson, M . A . (1996). Use of electromyogram telemetry to assess difficult passage areas for river-migrating adult sockeye salmon. Transactions of the American Fisheries Society 125: 253-260. Jain, K. E . , Birtwell, I. K . and Farrell, A . P. (1998). Repeat swimming performance of mature sockeye salmon following a brief recovery period: a proposed measure of fish health and water quality. Canadian Journal of Zoology 76: 1488-1496. Keen, J. E . and Farrell, A . P. (1994). Maximum prolonged swimming speed and maximum cardiac performance of rainbow trout, Oncorhynchus mykiss, acclimated to two different water temperatures. Comparitive Biochemistry and Physiology 108A: 287-295. 62 Lee, C . G . , Farrell, A . P., Lotto, A . , MacNutt, M . J. , Hinch, S. G . and Healey, M . C . (2003a). The effect of temperature on swimming performance and oxygen uptake in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks. Journal of Experimental Biology. 206:3239-3251. Lee, C . G . , Farrell, A . P., Lotto, A . , Hinch, S. G . and Healey, M . C . (2003b). Excess post-exercise oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks following critical speed swimming. Journal of Experimental Biology 206: 3253-3260. Macdonald, J. S. (2000). Mortality during the migration of Fraser River sockeye salmon (Oncorhynchus nerka): a study of the effect of ocean and river environmental conditions in 1997. Canadian Technical Report of Fisheries and Aquatic Sciences 2315. Fisheries and Oceans Canada. Burnaby, B C . Macdonald, J. S., Foreman, M . G . G . , Farrell, T. , Williams, I. V . , Grout, J. , Cass, A . , Woodey, J. C , Enzenhofer, H . , Clarke, W . C , Houtman, R., Donaldson, E . M . and Barnes, D. (2000). The influence of extreme water temperatures on migrating Fraser River sockeye salmon (Oncorhynchus nerka) during the 1998 spawning season. Canadian Technical Report of Fisheries and Aquatic Sciences 2326. Fisheries and Oceans Canada. Burnaby, B C . Milliken, C . (1983). Study of the metabolic rate in relation to swimming speed of adult pink salmon from the Fraser and Thompson Rivers. Contract OSB83-00375. Department of Fisheries and Oceans. Bamfield, B C . Morrison, J. , Quick, M . and Foreman, M . (2001). Climate change in the Fraser River watershed: flow and temperature predictions. Journal of Hydrology 263: 230-244. Rand, P. S. and Hinch, S. G . (1998). Swim speeds and energy use of upriver-migrating sockeye salmon (Oncorhynchus nerka): simulating metabolic power and assessing risk of energy depletion. Canadian Journal of Fisheries and Aquatic Science 55: 1832-1841. Randall, D. J . , Mense, D. and Boutilier, R. G . (1987). The effects of burst swimming on aerobic swimming in chinook salmon (Oncorhynchus tshawytscha). Marine Behaviour and Physiology 13: 77-88. Rome, L . C , Funke, R. P. and Alexander, R. M . (1990). The influence of temperature on muscle velocity and sustained performance in swimming carp. Journal of Experimental Biology 154: 163-178. Scarabello, M . , Heigenhauser, G . J. F. and Wood, C . M . (1992). Gas exchange, metabolite status and excess post-exercise oxxygen consumption after repetitive bouts of exhaustive exercise in juvenile rainbow trout. Journal of Experimental Biology 167155-169: Standen, E . M . (2001). Effects of hydraulic characteristics on energy use and behaviour of adult upriver migrating sockeye and pink salmon. M . Sc. thesis, University of British Columbia, Vancouver, B C . Standen, E . M . , Hinch, S. G . , Healey, M . C . and Farrell, A . P. (2002). Energetic costs of migration through the Fraser River Canyon, British Columbia, in adult pink (Oncorhynchus 63 gorbuscha) and sockeye (O. nerka) salmon assessed by E M G telemetry. Canadian Journal of Fisheries and Aquatic Science 59: 1809-1818. Tierney, K . (2000). The repeated swimming performance of sockeye, coho and rainbow trout in varying conditions. M.Sc. thesis, Simon Fraser University, Burnaby, B . C . Williams, I. V . and Brett, J . R. (1987). Critical swimming speed of Fraser and Thompson River pink salmon (Oncorhynchus gorbuscha). Canadian Journal of Fisheries and Aquatic Science 44: 348-356. Williams, I. V . , Brett, J. R., Bell, G . R., Traxler, G . S., Bagshaw, J. , McBride, J. R., Fagerlund, U . H . M . , Dye, H . M . , Sumpter, J. P., Donaldson, E . M . , Bilinski, E . , Tsuyuki, H . , Peters, M . D., Choromanski, E . M . , Cheng, J. H . Y . and Coleridge, W. L . (1986). The 1983 early run Fraser and Thompson River pink salmon; morphology, energetics and fish health. Bulletin. XXIII. 64 Appendix Table A3.1. Critical swimming speeds of adult pink and sockeye salmon that performed repeat ramp 20-minute UCRIT tests. Trial 1 and Trial 2 (Ucrit-i and U c r it-2 respectively) were separated by a 45-minute recovery at 0.45 FL-s"1. Recovery ratio (RR) is the quotient of UCrit-2/UCrit-i. The speed of gait transition from steady caudal fin swimming to consistent burst-coast swimming (U G T) is presented as a percent of UCRIT. Sex Temp <°C) Fork Length (cm) Ucrit-l (ems' Ucrit-2 ') Ucrit-1 (FL-s" Ucrit-2 RR 999 Pink Salmon S T N - 4 F 12.0 49.2 95.0 90.0 1.93 1.83 0.95 S T N - 7 F 12.0 53.9 112.7 124.0 2.09 2.3 1.10 STN-9 F 12.3 55.2 90.0 106.0 1.63 1.92 1.18 S T N - 2 M 11.5 49.6 95.2 98.7 1.92 1.99 1.04 STN-5 M 11.0 52.5 91.9 106.6 1.75 2.03 1.16 S T N - 8 M 11.5 55.1 99.2 173.6 1.8 3.15 1.75 STN-10 M 12.3 53.5 161.6 164.8 3.02 3.08 1.02 HGP-01 F 14.3 49.6 115.6 122.0 2.33 2.46 1.05 H G P - 0 2 F 13.5 50.8 141.7 102.6 2.79 2.02 0.73 H G P - 0 3 F 18.0 58.5 118.8 109.4 2.03 1.87 0.92 H G P - 0 5 M 18.5 50.0 96.5 111.0 1.93 2.22 1.15 H G P - 0 6 F 14.3 49.5 54.9 61.9 1.11 1.25 1.13 H G P - 0 7 M 17.5 59.0 115.1 1.95 H G P - 1 0 F 14.3 52.3 125.0 109.3 2.39 2.09 0.87 H G P - 1 2 M 20.0 58.4 141.3 165.3 2.42 2.83 1.17 H G P - 1 3 M 20.0 48.5 85.8 126.6 1.77 2.61 1.47 H G P - 1 4 M 20.3 51.6 81.0 98.6 1.57 1.91 1.21 H G P - 1 6 F 14.0 54.5 109.5 126.4 2.01 2.32 1.15 H G P - 1 7 F 10.0 50.0 45.5 0.91 H G P - 1 8 M 15.0 48.0 130.1 78.7 2.71 1.64 0.61 H G P - 1 9 M 18.0 51.0 124.4 127.0 2.44 2.49 1.02 H G P - 2 5 M 13.5 59.7 129.0 123.6 2.16 2.07 0.96 H G P - 2 6 F 19.0 52.5 120.2 116.0 2.29 2.21 0.96 H G P - 2 7 M 14.0 52.3 141.2 137.5 2.7 2.63 0.98 SP-01 M 16.0 52.0 75.9 76.4 1.46 1.47 1.01 SP-02 M 21.0 53.9 94.3 77.6 1.75 1.44 0.82 SP-03 F 16.0 57.3 154.7 158.7 2.7 2.77 1.03 SP-05 F 9.0 47.0 91.7 91.2 1.95 1.94 0.99 SP-06 F 21.0 48.5 108.6 128.0 2.24 2.64 1.18 SP-08 M 22.0 50.9 121.7 153.2 2.39 3.01 1.26 SP-09 F 13.0 53.3 98.1 86.9 1.84 1.63 0.89 SP-10 M 12.0 55.2 100.5 100.5 1.82 1.82 1.00 SP-11 F 12.0 53.4 90.8 70.5 1.7 1.32 0.77 SP-13 F 11.0 53.7 96.1 49.9 1.79 0.93 0.52 SP-14 F 16.0 52.6 118.9 113.6 2.26 2.16 0.96 65 SP-15 F 11.0 54.7 90.8 78.2 1.66 1.43 0.86 SP-19 F 17.0 53.0 134.6 128.8 2.54 2.43 0.96 2000 Sockeye Salmon YALE-00 14.3 64.9 152.5 157.1 2.35 2.42 1.03 YALE-01 13.6 55.0 127.1 128.7 2.31 2.34 1.01 YALE-02 12.2 53.9 136.4 140.1 2.53 2.6 1.03 YALE-03 12.3 55.9 130.2 114.0 2.33 2.04 0.88 YALE-04 12.8 57.9 130.9 137.2 2.26 2.37 1.05 YALE-05 13.2 59.5 142.8 144.0 2.4 2.42 1.01 2001 Sockeye Salmon ESS-00 M 12.5 61.0 124.4 142.1 2.04 2.33 1.14 ESS-01 M 12.0 57.4 107.9 117.7 1.88 2.05 1.09 ESS-02 F 16.0 57.7 155.8 154.6 2.7 2.68 1.00 ESS-03 F 16.0 57.1 143.9 152.5 2.52 2.67 1.06 ESS-04 F 20.0 65.4 117.7 111.8 1.8 1.71 0.95 ESS-05 F 20.0 60.1 137.0 150.3 2.28 2.5 1.09 ESS-06 M 11.5 63.5 116.2 103.5 1.83 1.63 0.89 ESS-07 M 12.0 59.1 104.0 72.7 1.76 1.23 0.70 ESS-08 M 14.0 62.1 106.8 80.7 1.72 1.3 0.75 ESS-09 F 18.0 59.0 120.4 139.2 2.04 2.36 1.16 For 20U1 pink salmon: H(jP individuals were collected at the Hell's Gate Fishway. SP individuals were collected at Seton Dam. 66 Chapter 4. Summary and Potential Ecological Relevance of Conclusions Research towards this thesis involved the measurement of complex performance parameters such as critical swimming speed and oxygen consumption. Although the proximate questions concerned differences in function (ie. physiology) among individuals and populations, my ultimate interest was in the ecological and evolutionary consequences of altered function or sub-optimal performance. Thesis summary We found that the differences in prolonged swimming ability (U c r i t ) between adult migrating pink and sockeye salmon were not as noteworthy as has been suggested throughout the literature (Brett 1982; Milliken 1983; Williams and Brett 1987; Heard 1991) and generally assumed by researchers, managers and fishers. Due to their larger size, sockeye salmon were able to attain slightly higher absolute swimming speeds but, when considered in FL-s" 1, critical swimming speeds were not significantly different between the species. Both species were equally able to repeat their first U c r j t performance following a 45-minute recovery period. Also contrary to other findings, our data suggested there were no differences in mean minimum or maximum metabolic rate (Mo2-min or Mo2-max, respectively) in pink and sockeye salmon. It had been previously assumed that sockeye salmon.possessed a maximum metabolic rate that was 30-40% higher than that of any other salmonids (Brett and Glass 1973). It had also been demonstrated that pink salmon exhibit higher resting metabolic rates, though this was attributed to the general "excitable" nature and of pink salmon in swimming tunnels (Milliken 1983; Williams et al. 1986). No evidence of such excitability in pink salmon behaviour was evident in this study either at the time of testing or upon review of the swimming videos. Like previous authors (Milliken 1983; Williams et al. 1986), however, we did find that metabolic rate across intermediate swimming speeds was significantly elevated in pink salmon as compared to sockeye salmon. This was attributed to both a higher tail beat frequency at a given swimming speed, and a higher oxygen cost of beating the tail at that frequency in pink salmon. Converting these data into measurements of cost of transport indicated that although pink salmon did display higher average costs of transport ( C O T a v e ) than sockeye salmon there were no between-species differences in minimum costs of transport ( C O T m i n ) . Thus by swimming at their optimal 67 swimming speed (-70 cm-s" ) pink salmon were able to swim as economically as sockeye salmon. Unlike the present study, comparisons in the past have been based on results of separate studies on pink and sockeye salmon. Therefore between-study differences in temperature, fish condition and maturity level, fish collection, holding and testing protocols, equipment used and personnel involved may have contributed to observed interspecific differences in swimming performance and metabolism. In general, temperature affected swimming performance and metabolism as expected. U c r j t showed a bell shaped curve with optimal performance at 15-16 °C in both species. Temperature dependence was weak (R 2 values < 0.2), however, and some individuals tested at extremes of the temperature range were capable of near equivalent performances to those tested at optimal temperatures. Both Mo2-min and Mo2-max increased with warming temperatures, as did the oxygen cost of swimming at intermediate speeds (in pink salmon only). A possible criticism of the methods used to evaluate temperature effects on swimming energetics surrounds the brief thermal acclimation periods employed in this study. Ideally fish should be given at least three weeks to fully acclimate to a temperature, before which any effects are generally considered acute. Due to restrictions related to working with senescing salmon, fish were allowed to acclimate for as little as 48 hours (up to 5 days) to experimental temperatures. However, results from Chapter 2 indicate that in a salmonid model, the cutthroat trout, acclimation processes occurred sufficiently rapidly that observed temperature effects on U c r i t - i and Ucrit-2 were the same on groups of fish that had acclimated for 48 hours or three weeks before testing (Figure 2.1). Thus, it was suggested that a minimum of 48 hours thermal acclimation was also sufficient to reveal acclimated, rather than acute effects of temperature on U c r i t in pink and sockeye salmon. No direct measurements of metabolism were recorded in the acclimation experiment discussed in Chapter 2. However, data on the recovery ratios (UCrit-2/UCnt-i) of fish from both brief and normal acclimation groups provide some insight into the rate at which fish can compensate for thermal effects on metabolic pathways. In cutthroat trout, the ability to recover from exhaustive exercise and repeat the initial U c r i t performance was not hindered by a brief thermal acclimation, and recovery ratio showed the same lack of relationship with temperature for both brief and normal acclimation groups (Figure 2.2). This suggests that 68 metabolic disturbances incurred from swimming to U c r j t , as well as the ability to recover and correct these disturbances are similar in fish that are acclimated for either 48 hours or three weeks. This discovery does not eliminate all possibility that fish in a state of partial thermal compensation may have influenced observed temperature effects on metabolism and energetic costs of swimming in pink and sockeye salmon. However, it does offer some reassurance that observed temperature effects were real. This work emphasizes that simply comparing means and regression lines may not always reveal important, ecologically relevant differences between groups of interest. For example, in Chapter 3, A N C O V A revealed no significant differences in Mo2-min or Mo2-max in magnitude or in response to temperature between pink and sockeye salmon. However, by visually examining the arrangement of the data it became quite clear that inter-individual variability in pink salmon was much greater than in sockeye salmon. Potential implications of species differences in inter-individual variation Of potentially equal ecological interest to the observed interspecific differences (or lack thereof) in the results from Chapter 3 are the consistent differences in intraspecific variation. The scatter in data points for swimming speed, Mo2-min, Mo2-max and metabolic scope are all much greater for pink than sockeye salmon across all temperatures. Even more obvious is the spread of total and net C O T for pink salmon as compared to sockeye salmon. In fact, measurements of U c r j t , M02-m a x , and C O T of what is considered a single stock-group of pink salmon more closely resembles the array of abilities exhibited by several stocks of sockeye salmon - from the relatively slow-swimming, energetically inefficient short distance migrating stocks, to the fast-swimming, exceptionally efficient long distance migrating stocks. Though variation in migratory behaviour may either compensate for or intensify the variation in swimming performance and energy efficiency within pink salmon, we suggest that the observed range may represent a real and mixed strategy of swimming physiologies within this species. These results contribute to mounting evidence suggesting that life history strategy may be quite different between pink and sockeye salmon. Consequently, there is a fundamental distinction in the organization of populations between these species. 69 The "stock-concept" (that individuals belong to discrete, self- perpetuating populations with distinct genotypes and phenotypes) has become a central concept to the management of fisheries. Sockeye salmon, in particular, are known to form genetically distinct units, isolated by strong fidelity to unique timing and location of spawning. Managers identify individual sockeye salmon to stock using allozymes, microsatellites, mtDNA, scale annuli and even migration run timing (Burgner 1991). It has been demonstrated that longer-distance migrating Fraser River sockeye salmon exhibit a higher critical swimming speed (U c r i t), higher maximum oxygen consumption (Mo2-max), a n ^ larger aerobic metabolic scope than shorter distance migrating sockeye (Lee et al. 2003a). Body constituent analyses of five stocks of Fraser River sockeye salmon also showed that fish from stocks facing more difficult migrations (based on distance and elevation) enter the river with greater energy stores and use the energy more efficiently than those undertaking less difficult migrations (Crossin 2002). However, such evidence of discrete pink salmon stocks is very weak, or lacking altogether. In the Fraser River, two general groups of pink salmon exist, an early migrating, upper river group (including fish examined in this study) and a later migrating, lower river group. Although a pink salmon can be identified as hatching from the Fraser River with reasonable accuracy, genetic homogeneity prevents identification of individuals to a finer scale (Bruce White, Pacific Salmon Commission, personal communication). Phenotypic homogeneity also prevails in pink salmon. Unlike sockeye salmon there are no morphological distinctions between upper and lower river pink salmon, and pink salmon undertaking migrations of varying difficulties all enter the river with identical energy levels and use the fuel in a similar manner en route to their spawning grounds (Crossin 2002). We suggest that pink salmon are not as locally adapted to migrations of a given duration or difficulty as sockeye salmon. Instead, the observed mix of abilities may allow pink salmon to be more of an exploratory species with their upriver destination less pre-programmed and more dependent on internal (fish health, energy stores) and external (river conditions, temperature, competition for spawning sites) environmental conditions. Due to the high energetic costs of undertaking long migrations, it is undesirable to do so unless fitness pay-offs are great. Thus, in years when conditions are good and access to suitable spawning habitat is relatively easy, there is no need to migrate several hundred kilometres upriver and individuals doing so will likely suffer losses in reproductive fitness. In these 'normal' years, weaker, less efficient swimmers will undoubtedly spawn successfully in the lower reaches of the river, contributing the genetic components of their swimming physiology to their offspring. However, when access to spawning 70 grounds is obstructed in some way or competition is intense, individuals capable of swimming farther upriver within their fixed energy budget may have greater reproductive success. Indeed, areas of spawning for pink salmon in the Fraser River have shown considerable density dependence, with thousands of individuals migrating as far as 1000 km to the Bowron River in years when numbers of spawners are high (Tracy Cone, Fisheries and Oceans Canada, Annacis Island, personal communication). These stronger and more efficient swimmers may be also be advantaged members of the population in terms of colonizing new habitats or re-colonizing spawning areas after obstructions to migration have been removed. Further support for this hypothesis comes from suggestions that pink salmon tend to stray and spawn away from natal streams more frequently than do sockeye and the other Pacific salmon species, probably contributing to their genetic and phenotypic homogeneity (Heard 1991). 71 Literature cited Bennett, A . F. (1990). Thermal dependence of locomotor capacity. American Journal of Physiology 259: R253-R258. Brett, J. R. (1982). The swimming speed of adult pink salmon, Oncorhynchus gorbuscha, at 20C and a comparison with sockeye salmon, O. nerka. Canadian Technical Report of Fisheries and Aquatic Sciences. 1143. Brett, J. R. and Glass, N . R. (1973). Metabolic rates and critical swimming speeds of sockeye salmon (Oncorhynchus nerka) in relation to size and temperature. Journal of the Fisheries Research Board of Canada 30: 379-387. Burgner, R. L . (1991). Life History of Sockeye Salmon (Oncorhyncus nerka). In Pacific Salmon Life Histories. Edited by L . Margolis. U B C Press, Vancouver, B C , Canada, pp. 3-117. Crossin, G . T. (2002). Effects of ocean climate and upriver migratory constraints on the bioenergetics, fecundity, and morphology of wild, Fraser River salmon. M . S c , University of British Columbia, Vancouver. Heard, W. R. (1991). Life History of Pink Salmon (Oncorhyncus gorbuscha). In Pacific Salmon Life Histories. Edited by L . Margolis. U B C Press, Vancouver, B C . pp. Lee, C. G . (2002). Swimming performance, metabolic rate and recovery of adult Pacific salmon (Oncorhynchus spp.). M.Sc. thesis, Simon Fraser University, Burnaby. Milliken, C . (1983). Study of the metabolic rate in relation to swimming speed of adult pink salmon from the Fraser and Thompson Rivers. Contract OSB83-00375. Department of Fisheries and Oceans. Bamfield, B C . Williams, I. V . and Brett, J . R. (1987). Critical swimming speed of Fraser and Thompson River pink salmon (Oncorhynchus gorbuscha). Canadian Journal of Fisheries and Aquatic Science 44: 348-356. Williams, I. V . , Brett, J. R., Bell, G . R., Traxler, G . S., Bagshaw, J. , McBride, J. R., Fagerlund, U . H . M . , Dye, H . M . , Sumpter, J. P., Donaldson, E . M . , Bilinski, E . , Tsuyuki, H . , Peters, M . D., Choromanski, E . M . , Cheng, J. H . Y . and Coleridge, W . L . (1986). The 1983 early run Fraser and Thompson River pink salmon; morphology, energetics and fish health. Bulletin. XXIII. 72 

Cite

Citation Scheme:

        

Citations by CSL (citeproc-js)

Usage Statistics

Share

Embed

Customize your widget with the following options, then copy and paste the code below into the HTML of your page to embed this item in your website.
                        
                            <div id="ubcOpenCollectionsWidgetDisplay">
                            <script id="ubcOpenCollectionsWidget"
                            src="{[{embed.src}]}"
                            data-item="{[{embed.item}]}"
                            data-collection="{[{embed.collection}]}"
                            data-metadata="{[{embed.showMetadata}]}"
                            data-width="{[{embed.width}]}"
                            async >
                            </script>
                            </div>
                        
                    
IIIF logo Our image viewer uses the IIIF 2.0 standard. To load this item in other compatible viewers, use this url:
http://iiif.library.ubc.ca/presentation/dsp.831.1-0090958/manifest

Comment

Related Items