© 2001 by The Society for Integrative and Comparative Biology
Terrestrial Intermittent Exercise: Common Issues for Human Athletics and Comparative Animal Locomotion1
1 Department of Physiology, 1501 N. Campbell Avenue, University of Arizona, Tucson, Arizona 85724
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The earliest studies of intermittent exercise physiology noted that moving intermittently (i.e., alternating brief movements with brief pauses) could transform a heavy workload into a submaximal one that can be tolerated and sustained. The brief pauses that characterize intermittent locomotion permit at least partial recovery from prior activity. This research provided the foundation for the development of interval training and more recently for the re-evaluation of steady-state paradigms for comparative animal locomotion. In this paper I review key concepts underlying the performance of repeated activity. I provide examples from human athletics and training and comparative animal locomotion. To explore the limits of intermittent exercise performance, I examine the performance limits for continuous exercise and the rate and extent of the recovery of performance capacity following activity. While it is evident that altering locomotor behavior (i.e., moving intermittently) can alter the capacity of an animal to perform work, mathematical models of intermittent exercise could predict strategies (i.e., exercise intensity, exercise duration, and pause duration) that will increase performance limits for intermittent activity.
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INTRODUCTION |
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Continuous, steady-state exercise has played an essential role in defining the limits of locomotor performance. Energy demand, oxygen transport, and biomechanics of musculo-skeletal systems are well-documented during steady-state, constant speed locomotion. Yet, as suggested by Astrand and Rodahl (1977)
, steady-state conditions represent "an artificial situation for many animals." Few animals move continuously; instead, most start and stop frequently. As a result, their physiological and biomechanical systems must function under non-steady-state, transient conditions. Therefore, we should re-evaluate the capacity of biomechanical and physiological systems with respect to repeated activity to advance our understanding of systems design, function, and control.
By integrating several levels of biological organization, including behavior, physiology, biomechanics and biochemistry, we can discover new principles of locomotor performance. One such principle is that altering behavior (i.e., the way in which bouts of activity or work are distributed over time) can alter the capacity of an individual to perform work. In the 1960s, Scandinavian exercise physiologists noted that when a heavy (i.e., supramaximal) workload is divided into short exercise and pause periods, the heavy workload is "transformed to a submaximal load on circulation and respiration and [can be] well tolerated" (Astrand et al., 1960). More recently, this concept has been demonstrated in comparative activity physiology. Moving intermittently alters performance limits compared to continuous locomotion in semi-terrestrial crabs (Weinstein and Full, 1992, 1998, 2000), cockroaches (Weinstein and Full, 2000), and a lizard (Weinstein and Full, 1999). Specifically, moving intermittently at a speed greater than the maximum aerobic speed (MAS; i.e., the minimum speed at which the maximal rate of oxygen consumption, 
O2max, is attained) can increase the total distance traveled before exhaustion by 6- to 11-fold compared to moving continuously at the same speed (Weinstein and Full, 1992, 1998, 1999, 2000). More interestingly, the total distance traveled before exhaustion can be increased by 2- to 5-fold compared to the distance traveled by moving continuously at the same average speed, even when the average speed is less than the MAS (Weinstein and Full, 1992, 1998, 1999, 2000). It is important to note that moving intermittently does not always increase performance. Some movement and pause regimes can reduce the distance traveled before exhaustion to one-tenth of that for continuous locomotion at the same average speed (Weinstein and Full, 1992, 2000).
In this paper I will explore the basic premise of intermittent exercise physiology (i.e., that altering behavior can alter the capacity of an individual to perform work) in relation to both human exercise physiology and comparative activity physiology. I will begin by providing examples of intermittent locomotion from human athletics and animal behavior studies. Next, I will evaluate total work output prior to exhaustion for intermittent locomotion, which is determined by the exercise intensity, exercise duration, and pause duration. To do this, I will first examine the limits to performance during a single bout of activity. Then I will describe recovery from prior activity and its relation to the performance of subsequent activity and thus intermittent exercise. Finally, I will discuss the implications for future comparative studies of intermittent locomotion.
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INTERMITTENT ACTIVITY IN ATHLETICS AND ANIMAL BEHAVIOR |
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Intermittent exercise, which is characterized by frequent periods of intense work followed by periods of less-intense recovery (Christmass et al., 1998), reflects the nature of many physical occupations (e.g., smelters working in an ironwork, delivery persons carrying heavy boxes up flights of stairs, farmers, gardeners; Saltin et al., 1976). It is also the basis of multi-sprint sports (e.g., soccer, tennis, basketball, handball, and ice hockey; see Alexander and Boreskie, 1989
; Bangsbo, 1994; Christmass et al., 1998; Green et al., 1976; McInnes et al., 1995).
Sports involving intermittent exercise illustrate the principle that frequent pauses can transform a high-intensity workload into a submaximal physiological load by permitting at least partial recovery from prior activity. During a soccer match, players must frequently switch between many different activities, including high-intensity running and sprinting which would rapidly lead to exhaustion if performed continuously. Time-motion analysis indicates that top-level players travel approximately 11 km in a 90 min match (Bangsbo, 1994), with players engaging in high-intensity running or sprinting for about 8% of the total playing time (Bangsbo et al., 1991). Each high-intensity bout is brief, averaging 2 sec, and is interspersed with frequent periods of standing or walking, averaging 7 sec (Bangsbo et al., 1991). Degradation of creatine phosphate provides energy during intense exercise periods but it is rapidly re-synthesized during periods of rest and low-intensity exercise such that the creatine phosphate concentration probably oscillates throughout a match due to the intermittent nature of the game (Bangsbo, 1994). Despite frequent high-intensity bouts, it is estimated that the average work rate during a match is approximately 70% of o2max, with aerobic energy production accounting for more than 90% of the total energy consumption (Bangsbo, 1994).
Interval training is a direct application of the fundamental principles of intermittent exercise. The basis for interval training is that when short periods of rest are alternated with periods of high-intensity exercise, "the total accumulated exercise time can be greatly increased beyond that which could be achieved during a single continuous bout at the same intensity to exhaustion" (MacDougall and Sale, 1981). Interval training allows athletes to refine and practice their technique because intermittent bouts of exercise and recovery permits them to train in the absence of fatigue (Daniels and Scardina, 1984). Pause intervals should be long enough so the athlete can perform at the same intensity during subsequent exercise intervals. However, if the pause intervals are too long, physiological systems will not be stressed enough to induce a training effect (Martin and Coe, 1997). An interval training program should be designed according to the specific needs of the individual athlete. By varying exercise intensity, exercise duration, and recovery duration, coaches and athletes can tailor workouts to improve either anaerobic power or aerobic capacity.
A competitive race that relies on the basic principles of intermittent exercise is the ride and tie (Johns, 1985). Ride and tie is a long distance race over cross-country trails involving teams of one horse and two humans. At the start of the race, one person rides the horse a pre-arranged distance of the team's choice, ties the horse to a tree, and begins running. Meanwhile, the other runner catches up to the horse, unties it and begins riding. The humans alternate running and riding throughout the race while the horse alternates running and resting (i.e., being tied). A team completes the race when all three team members cross the finish line. Each team is required to make a minimum of 6 ties during the race, including 3 to 4 mandatory veterinary checks spaced throughout the race. Horses cannot leave the veterinary check if they exceed pulse (
72 beats/min) and respiration rate (72 breaths/min) criteria. Most teams make 30 to 40 ties over a 60 km (40 mile) course, presumably to allow each individual to maximize their speed over short intervals by interspersing brief recovery bouts. Thus, the long distance race is broken down into several shorter distance segments with frequent recovery periods, enabling the team to maximize speed over the total race distance.
While the fundamental principles of intermittent exercise have important applications for human athletics and training, the same principles have implications for the locomotor behavior of animals. Locomotion is important for survival and fitness as animals move to forage, escape predators and search for mates. In addition, locomotion can represent a significant fraction of an animal's total energy budget. O'Brien et al. (1990) and McLaughlin (1989) propose a continuum of locomotor patterns for foraging animals. The constant motion of cruising foragers (e.g., hawk) and the ambush tactics of sit-and-wait predators (e.g., lion) lie at the extremes of this continuum. Most animals occupy an intermediate position, displaying what O'Brien and co-workers call a "saltitory" search mode (1990). Intermittent foraging patterns are exhibited by a wide range of animals, including copepods (Vanduren and Videler, 1995), semi-terrestrial crabs (Weinstein, 1995), birds (Cody, 1968), lizards (Huey and Pianka, 1981), fish (Evans and O'Brien, 1988; O'Brien et al., 1979, 1990) and mammals (Kenagy and Hoyt, 1989; McAdam and Kramer, 1998).
Moving intermittently may increase both the time required to travel a given distance and the energetic cost of locomotion but these disadvantages may be counteracted by benefits including increased prey detection, increased predator detection (vigilance), reduced attack rate by predators, and increased distance traveled before exhaustion (McAdam and Kramer, 1998). With regard to the distance traveled before exhaustion, intermittent locomotion can have greater consequences for ectotherms than endotherms. Moving intermittently may either reduce the limitations associated with the low o2max and MAS characteristic of ectotherms or, alternatively, impose additional constraints (Weinstein and Full, 1992).
Ectotherms often move at speeds that are greater than their MAS, but their locomotion is punctuated by frequent pauses (Garland, 1985; Weinstein, 1995). The pauses may provide time for at least partial recovery from the metabolic demands of prior high-intensity movement bouts, as suggested by low lactate accumulation of foraging animals (Gatten, 1985; Johnson, 1987). I recorded movements of individual ghost crabs in their natural habitat by focal animal sampling and three-dimensional motion analysis to quantify the intermittent movements of voluntarily active and stressed (i.e., captured and released into the study site) crabs (Weinstein, 1995). On average, the stressed crabs moved at faster speeds than voluntarily active crabs, although both groups of crabs moved at speeds that sometimes exceeded their MAS. I predicted that the stressed crabs would pause a greater proportion of the time to recover from their more frequent, shorter duration, and higher-intensity movements than voluntarily active crabs. To test this prediction, I measured the mean duration of movements and pauses from videotaped focal animal sampling observations. I estimated the speed of each movement from stride frequency, since stride frequency is directly proportional to speed at stride frequencies less than 6 Hz (Blickhan and Full, 1987). I found that voluntarily active crabs spent less than 2.4% of their time moving at speeds greater than their MAS (a stride frequency of approximately 3 Hz; Blickhan and Full, 1987; Full, 1987), while most of their movements were of lower intensity (31.6% of the total time; Fig. 1A). In contrast, stressed crabs moved at speeds greater than their MAS 16.1% of the observation time, even though moving continuously at these speeds would rapidly lead to exhaustion, while moving at slower speeds only 7.3% of the total time (Fig. 1B). As predicted, the stressed crabs paused a greater proportion of the time (76.6%) than the voluntarily active crabs (66.0%; Fig. 1). While this analysis does not discount other behavioral advantages of moving intermittently, the results indicate that stressed crabs use a greater proportion of time for metabolic recovery from high-intensity activity, a mechanism which appears to increase their locomotor performance limits.
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PERFORMANCE LIMITS FOR A SINGLE BOUT OF ACTIVITY |
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Altering locomotor behavior (i.e., movement intensity, movement duration, and pause duration) can alter the capacity of an animal to perform work and the load on physiological systems, as illustrated in the above examples from human athletics and comparative animal studies. To define the limits of this effect, we must we must first establish a baseline for comparison by quantifying performance limits for continuous locomotion. Total work output is determined by the intensity and duration of each work bout and the duty cycle, defined as the % of total time spent moving. In this section, I will consider the case of continuous exercise (duty cycle = 100%). Therefore, the aim of this section is to examine the performance limits for a single, continuous bout of activity.
How much work can be accomplished before exhaustion during continuous exercise? To address this question, we can measure the total external work done by a subject or the amount of work done per unit time (i.e., power). The measure of performance may be task-specific. For example, if we are studying cycling performance, we could measure average power output or total work output. If we are examining running performance, we could measure average speed or total distance. For terrestrial organisms ranging from bipeds to polypeds, the rate of mechanical work (i.e., power) required to move the center of mass increases linearly with speed and thus the amount of work done is proportional to the distance traveled (Full, 1989). Exhaustion can be defined as the inability to sustain exercise at a target intensity to distinguish it from fatigue, which is a decline in force-generating capacity (Vollestad et al., 1988). Therefore, fatigue is a gradual process that begins at the onset of exercise but the limit to performance is identified when the subject becomes exhausted.
Endurance (time to exhaustion) curves represent the upper limit for power output during a single bout of continuous exercise (Fig. 2). For both running and cycling, exercise at low power outputs, which is fueled primarily by oxidative ATP production, can be sustained for long periods of time while exercise at high power outputs, which requires additional ATP production from non-oxidative sources, rapidly leads to exhaustion. Based on world records, the fastest average speed a person can sustain for 19 sec is 37.2 km/hr but an average speed of 23.3 km/hr can be sustained for 25.8 min (Fig. 2A). Endurance curves based on world records could be misleading since each data point represents a different individual. However, the same general pattern emerges when endurance curves are constructed for single individuals (Fig. 2A). A lower o2max will contribute to a leftward shift of the endurance curve (Gatten et al., 1992). For ectotherms, such as the ghost crab, a decline in body temperature (Tb) from 24 to 15°C decreases o2max and MAS and as a result shifts the endurance curve to the left (Fig. 2D; Weinstein and Full, 1994).
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We can use endurance curves to make predictions about continuous locomotor performance. To maximize total work output (or total distance traveled) before exhaustion during continuous locomotion, exercise should be carried out at a low power output (e.g., at speeds/power outputs to the left of the endurance curves in Fig. 2). However, to maximize total work output (or distance traveled) in a given amount of time, exercise should be carried out at the maximum work rate (or speed) that can be sustained for that time period (i.e., a point on the endurance curve; Fig. 2). These predictions assume that work is performed continuously. If the work is performed intermittently, then predictions should address the possible advantages of recovery from prior activity and the potential trade-off between recovery time and power output.
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RECOVERY FROM PRIOR ACTIVITY AND THE PERFORMANCE OF SUBSEQUENT ACTIVITY |
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When movement is intermittent, the pause period may permit recovery from prior activity but what is the minimum pause needed for complete recovery of performance? Several factors influence the extent and rate of recovery including the intensity and duration of prior activity, the type of exercise, whether recovery is active and passive, and, for ectotherms in particular, body temperature (Tb).
There are several methods to assess the extent and rate of recovery. First, we can measure the recovery of the capacity to generate force or power. This can be done by stimulating muscle electrically or asking the subject to perform a voluntary contraction or effort and measuring force or power at various time points during recovery (e.g., Hitchcock, 1989; Stull and Clarke, 1971). Recovery of performance would be complete when the force or power return to pre-exercise levels. Second, we can measure the recovery of the capacity to sustain a given workload. At various times during the recovery period, the subject could be asked to repeat the exercise task (e.g., Stull and Kearney, 1978). Recovery of performance would be complete when the mean power output or endurance during the second exercise bout is the same as in the first exercise bout. Alternatively, the subject could be asked to repeat an exercise task one or more times with a specified pause interval (e.g., Balsom et al., 1992a, b). If the task can be repeated without a decline in average power output from one exercise interval to the next then the pause interval permits complete recovery of performance. Several studies show that recovery of force and endurance follow a two- or three-component exponential pattern with at least an initial rapid component and a delayed slow component (Hitchcock, 1989; Stull and Clarke, 1971; Stull and Kearney, 1978). The recovery of endurance is slower than the recovery of strength (i.e., force; Stull and Kearney, 1978).
One general pattern that emerges from the literature is that as exercise intensity increases, a larger recovery ratio (recovery duration/exercise duration) is needed for complete recovery of performance (Fig. 3). For example, complete recovery of pre-exercise maximum leg extension torque after 120 sec of cycling at 120% o2max required 8 min but only 1 min was needed for complete recovery from 120 sec of cycling at 80% o2max (Fig. 3A; Hitchcock, 1989). In terms of intermittent exercise, this means the duty cycle must decrease as exercise intensity increases if the exercise is to be repeated without a decline in performance.
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Interval training tables also suggest that the minimum recovery ratio increases as exercise intensity increases. Interval training tables recommend the minimum recovery duration "to ensure that the athlete can complete each interval at the assigned pace while maintaining good form" (Martin and Coe, 1997
). For longer duration, slower-paced intervals, the minimum recovery is considerably shorter than the run duration, but for very short duration, faster-paced intervals "a far longer time that that required to run the interval distance may be appropriate" (Martin and Coe, 1997). According to a popular interval training table (Martin and Coe, 1997), when the running interval is 10 to 30 sec and the running speed is the maximum pace that can be sustained over the running interval (i.e., corresponding to 35 to 37 km/hr for a world record holder), the recovery duration should be 3 times as long as the running interval (Fig. 3B, C). However, when the running interval is 4 to 20 min and the running speed is 80% of the maximum pace that can be sustained over the running interval (i.e., corresponding to 15 to 21 km/hr for a world record holder), the recovery duration needs to be only half as long as the running interval (Fig. 3B, C).
Two additional lines of evidence support the increase in minimum recovery ratio as exercise intensity increases. First, Balsom and co-workers (1992a) found that the minimum sprint time over 40 m (an average of 5.58 sec) did not change when alternated with 120 sec rest periods but sprint time increased significantly when alternated with 30 sec rest periods and increased slightly when alternated with 60 sec rest periods. These results suggest that the minimum recovery time is approximately 10 to 20 times as long as the high-intensity run duration. At the other end of the spectrum, many ultra-distance runners use a racing strategy that alternates 15 to 25 min of running with 5 min of walking (Lathan and Cantwell, 1981; Osler and Dodd, 1979), suggesting that longer, lower intensity intervals decrease the minimum recovery time to approximately 20–33% of the running duration.
Moderate aerobic work during the recovery interval may speed the rate of recovery. In a study where subjects alternated 6 sec of maximal effort cycling with 30 sec of either passive (sitting motionless on the seat) or active (cycling at 60 rpm against 1 kg resistance) recovery, the peak power and total work completed during subsequent exercise intervals was higher following active rather than passive recovery periods (Signorile et al., 1993). While active recovery involving limbs used during the exercise interval has beneficial effects, "diverting activities" can also improve performance during subsequent work bouts (Asmussen and Mazin, 1978). In one study that illustrates the benefit of "diverting activities," the amount of work that could be performed by one arm during repeated exercise bouts was higher when the subjects performed exercise with the contralateral arm during the recovery intervals (Asmussen and Mazin, 1978). There is considerable information in the literature regarding the positive impact of an active versus passive recovery interval on lactate removal and even the workload that maximizes the rate of lactate removal. Hermansen and Stensvold (1972) compared a resting recovery to active recoveries at 30 to 80% of o2max and found that the greatest rate of lactate removal occurred at 63% o2max. However, it should be noted that there is evidence that moderate lactate accumulation is not a primary determinant of subsequent exercise performance (e.g., Balsom et al., 1992a).
Body temperature has an effect on the rate of recovery and is therefore expected to have major consequences for intermittent locomotor performance, especially in ectotherms. Temperature affects many physiological systems that can influence locomotor performance, including the muscles that power locomotion, the nervous system that controls the muscles, and the circulatory and respiratory systems that supply oxygen and nutrients to the muscles. In general, a decrease in Tb decreases o2max and the MAS and slows the kinetics of turning on and off physiological systems (e.g., Gleeson, 1980; Wagner and Gleeson, 1996; Weinstein and Full, 1994, 1998). Several studies have measured the recovery of the capacity to generate force in the muscle fibers of ectotherms at a single temperature (e.g., Fitts and Holloszy 1976) but fewer studies have compared the rates of recovery of at different temperatures (e.g., Lannergren and Westerblad, 1988). Recovery of whole-animal locomotor performance capacity at different Tb's would be an important area for future research.
Intermittent locomotor performance at low Tb will depend on the interplay between reduced energy demand and slowed kinetics, and this interaction appears to be complex. Ghost crabs with a Tb of 24°C alternating 30 sec of exercise at 166% MAS with 30 sec pause periods can cover 71% less distance before exhaustion compared to continuous locomotion at the same average speed (83% MAS; Weinstein and Full, 1992). However, at a Tb of 15°C, moving intermittently at the same exercise intensity (166% MAS), exercise duration (30 sec), and pause duration (30 sec) increases distance capacity by 4.5-fold compared to continuous locomotion at the same average speed (Weinstein and Full, 1998). Conversely, an intermittent exercise regime that enhances performance at a Tb of 24°C (120 sec at 166% MAS alternated with 120 sec pauses) reduces performance at 15°C (Weinstein and Full, 1998). Taken together, these data suggest that the minimum recovery ratio needed for the complete recovery of performance is not only dependent upon exercise intensity but also Tb. At present, there is not enough information in the literature to make more specific predictions about the effect of temperature on intermittent locomotor performance so this would be a promising area for future research.
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IMPLICATIONS FOR FUTURE STUDIES OF INTERMITTENT LOCOMOTION |
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Altering locomotor behavior can alter the capacity of an animal to perform work, but which strategies will lead to the largest increase or decrease in performance? In terms of maximizing the total amount of work done per unit time, there appears to be a trade-off between the maximum power output that can be achieved during an exercise bout and the minimum recovery ratio. As the intensity of the exercise bouts increases during intermittent locomotion, longer pause periods are needed, and therefore the duty cycle must be decreased. A lower duty cycle will in turn decrease the average power output per unit time for intermittent exercise. Future mathematical models of intermittent exercise performance should help to identify the strategies which will maximize work per unit time, minimize the time needed to complete a given amount of work, or maximize total work output before exhaustion. Future laboratory studies should examine the underlying physiological mechanisms that determine performance limits. Ultimately, the integration of laboratory and field studies of intermittent locomotor performance will reveal novel principles of systems design, function, and control.
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ACKNOWLEDGMENTS |
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I thank Bob Full, John Hartman, and an anonymous reviewer for their insightful comments. I also thank Mack Eleid and Jennifer Raymond for their assistance with the preparation of this manuscript.
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FOOTNOTES |
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1 From the Symposium on Intermittent Locomotion: Integrating the Physiology, Biomechanics and Behavior of Repeated Activity presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2000, at Atlanta, Georgia.
2 E-mail: randiw{at}cs.arizona.edu
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Alexander, M. J. L., and S. L. Boreskie. 1989. An analysis of fitness and time-motion characteristics of handball. Am. J. Sports Med, 17:76-82.
Asmussen, E., and B. Mazin. 1978. Recuperation after muscular fatigue by "diverting activities.". Europ. J. Appl. Physiol, 38:1-7.
Astrand, I., P.-O. Astrand, E. H. Christensen, and R. Hedman. 1960. Intermittent muscular work. Acta Physiol. Scand, 48:448-453.[Web of Science][Medline]
Astrand, P.-O., and K. Rodahl. 1977. Textbook of work physiology. 2nd ed. McGraw-Hill, New York.
Balsom, P. D., J. Y. Seger, B. Sjodin, and B. Ekblom. 1992a. Maximal-intensity intermittent exercise: Effect of recovery duration. Int. J. Sports Med, 13:528-533.[Web of Science][Medline]
Balsom, P. D., J. Y. Seger, B. Sjodin, and B. Ekblom. 1992b. Physiological responses to maximal intensity intermittent exercise. Eur. J. Appl. Physiol, 65:144-149.[CrossRef][Web of Science]
Bangsbo, J. 1994. The physiology of soccer with special reference to intense intermittent exercise. Acta Physiol. Scand. Suppl, 619:1-155.[Medline]
Bangsbo, J., L. Norregaard, and F. Thorso. 1991. Activity profile of competition soccer. Can. J. Spt. Sci, 16:110-116.
Billat, L. V., J. P. Koralsztein, and R. J. Morton. 1999. Time in human endurance models: From empirical models to physiological models. Sports Med, 27:359-379.[CrossRef][Web of Science][Medline]
Blickhan, R., and R. J. Full. 1987. Locomotion energetics of the ghost crab. II. Mechanics of the centre of mass during walking and running. J. Exp. Biol, 130:155-174.
Christmass, M. A., S. E. Richmond, N. T. Cable, P. G. Arthur, and P. E. Hartmann. 1998. Exercise intensity and metabolic response in singles tennis. J. Sports Sci, 16:739-747.[CrossRef][Web of Science][Medline]
Cody, M. I. 1968. On the methods of resource division in grassland bird communities. Am. Nat, 102:107-147.[CrossRef][Web of Science]
Daniels, J., and N. Scardina. 1984. Interval training and performance. Sports Med, 84:327-334.
Ekblom, B. 1986. Applied physiology of soccer. Sports Med, 3:50-60.[Web of Science][Medline]
Evans, B. I., and W. J. O'Brien. 1988. A re-analysis of the search cycle of a planktivorous salmonid. Can. J. Fish. Aquat. Sci, 45:187-192.
Fitts, R. H., and J. O. Holloszy. 1976. Lactate and contractile force in frog muscle during development of fatigue and recovery. Am. J. Physiol, 231:430-433.
Full, R. J. 1987. Locomotion energetics of the ghost crab. I. Metabolic cost and endurance. J. Exp. Biol, 130:137-153.
Full, R. J. 1989. Mechanics and energetics of terrestrial locomotion: From bipeds to polypeds. In W. Wieser and E. Gnaiger (eds.), Energy transformation in cells and animals, pp. 175–182. Thieme, Stuttgart.
Garland, T. 1985. Physiological and Ecological Correlates of Locomotory Performance and Body Size in Lizards, Chapter 5. Ph.D. Diss.,. University of California, Irvine.
Gatten, R. E., Jr. 1985. The uses of anaerobiosis by amphibians and reptiles. Amer. Zool, 25:945-954.
Gatten, R., K. Miller, and R. J. Full. 1992. Locomotion energetics at rest and during exercise. In M. E. Feder and W. Burggren (eds.), Environmental physiology of the amphibians, pp. 314–377. Cambridge University Press, New York.
Gleeson, T. T. 1980. Metabolic recovery from exhaustive activity by a large lizard. J. Appl. Physiol, 48:689-694.
Green, H., P. Bishop, M. Houston, R. McKillop, R. Norman, and P. Stothart. 1976. Time-motion and physiological assessments of ice hockey performance. J. Appl. Physiol, 40:159-163.[Web of Science][Medline]
Hermansen, L., and I. Stensvold. 1972. Production and removal of lactate during exercise in man. Acta Physiol. Scand, 86:191-201.[Web of Science][Medline]
Hitchcock, H. C. 1989. Recovery of short-term power after dynamic exercise. J. Appl. Physiol, 67:677-681.
Huey, R. B., and E. R. Pianka. 1981. Ecological consequences of foraging mode. Ecology, 62:991-999.[CrossRef][Web of Science]
Hughson, R. L., C. J. Orok, and L. E. Staudt. 1984. A high velocity treadmill running test to assess endurance running potential. Int. J. Sports Med, 5:23-25.[Web of Science][Medline]
Johns, B. 1985. What is this madness? Synergistic Press, San Francisco.
Johnson, B. A. 1987. Structure and function of the hemocyanin from a semi-terrestrial crab, Ocypode quadrata. J. Comp. Physiol, 157:501-509.[CrossRef]
Kenagy, G. J., and D. F. Hoyt. 1989. Speed and time-energy budget for locomotion in golden-mantled ground squirrels. Ecology, 70:1834-1839.[CrossRef]
Lannergren, J., and H. Westerblad. 1988. The effect of temperature and stimulation scheme on fatigue and recovery in Xenopus muscle fibres. Acta Physiol. Scand, 133:73-82.[Web of Science][Medline]
Lathan, S. R., and J. D. Cantwell. 1981. A run for the record: Studies on a trans-American ultramarathoner. JAMA, 245:367-368.
MacDougall, D., and D. Sale. 1981. Continuous vs. interval training: A review for the athlete and the coach. Can. J. Appl. Spt. Sci, 6:93-97.
Martin, D. E., and P. N. Coe. 1997. Better training for distance runners. Human Kinetics, Champaign, Illinois.
McAdam, A. G., and D. L. Kramer. 1998. Vigilance as a benefit of intermittent locomotion in small mammals. Anim. Behav, 55:109-117.[CrossRef][Web of Science][Medline]
McInnes, S. E., J. S. Carlson, C. J. Jones, and M. J. McKenna. 1995. The physiological load imposed on basketball players during competition. J. Sports Sci, 13:387-397.[Medline]
McLaughlin, R. L. 1989. Search modes op birds and lizards: Evidence for alternative movement patterns. Amer. Nat, 133:654-670.[CrossRef][Web of Science]
O'Brien, W. J., B. I. Evans, and H. I. Brownman. 1979. Flexible search tactics and efficient foraging in saltatory searching animals. Oecologia, 80:100-110.[CrossRef]
O'Brien, W. J., H. I. Brownman, and B. I. Evans. 1990. Search strategies of foraging animals. Amer. Sci, 78:152-160.
Osler, T., and E. Dodd. 1979. Ultra-marathoning: The next challenge. World Publications, Inc., Mountain View, California.
Saltin, B., B. Essen, and P. K. Pedersen. 1976. Intermittent exercise: Its physiological and some practical applications. In E. Jokl (ed.), Medicine and sport: Advances in exercise physiology, pp. 23–51. Karger, Basel.
Signorile, J. F., C. Ingalls, and L. M. Tremblay. 1993. The effects of active and passive recovery on short-term, high intensity power output. Can. J. Appl. Physiol, 18:31-42.[Web of Science][Medline]
Stull, G. A., and D. H. Clarke. 1971. Patterns of recovery following isometric and isotonic strength decrement. Med. Sci. Sports, 3:135-139.[Medline]
Stull, G. A., and J. T. Kearney. 1978. Recovery of muscular endurance following submaximal, isometric exercise. Med. Sci. Sports, 10:109-112.[Web of Science][Medline]
Vanduren, L. A., and J. J. Videler. 1995. Swimming behaviour of developmental stages of the calanoid copepod Temora longicornis at different food concentrations. Marine Ecology-Progress Series, 126:153-161.
Vollestad, N. K., O. M. Sejersted, R. Bahr, J. J. Woods, and B. Bigland-Ritchie. 1988. Motor drive and metabolic responses during repeated submaximal contractions in humans. J. Appl. Physiol, 64:1421-1427.
Wagner, E. L., and T. T. Gleeson. 1996. Low temperature and exercise recovery in the desert iguana. Physiol. Zool, 69:168-190.
Weinstein, R. B. 1995. Locomotor behavior of nocturnal ghost crabs on the beach: Focal animal sampling and instantaneous velocity from three-dimensional motion analysis. J. Exper. Biol, 198:989-999.[Medline]
Weinstein, R. B., and R. J. Full. 1992. Intermittent exercise alters endurance in an eight-legged ectotherm. Am. J. Physiol, 262:R852-R859.[Medline]
Weinstein, R. B., and R. J. Full. 1994. Thermal dependence of locomotor energetics and endurance capacity in the ghost crab, Ocypode quadrata. Physiol. Zool, 67:855-872.
Weinstein, R. B., and R. J. Full. 1998. Performance limits of low-temperature, continuous locomotion are exceeded when locomotion is intermittent in the ghost crab. Physiol. Zool, 71:274-384.[Medline]
Weinstein, R. B., and R. J. Full. 1999. Intermittent locomotion increases endurance in a gecko. Physiol. Biochem. Zool, 72:732-739.[CrossRef][Web of Science][Medline]
Weinstein, R. B., and R. J. Full. 2000. Intermittent locomotor behaviour alters total work. In P. Domenici and R. W. Blake (eds.), Biomechanics in animal behaviour, pp. 33–48. BIOS Scientific, Oxford.
Wilkie, D. R. 1980. Equations describing power input by humans as a function of duration of exercise. In P. Cerretelli and B. J. Whipp (eds.), Exercise bioenergetics and gas exchange, pp. 75–80. North-Holland Biomedical Press, Elsevier.
Wright, J. W.(ed.) 1998. The New York Times 1999 Almanac. Penguin Reference Books, New York.
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