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Biomechanical assessment of adaptive radiation in threespine sticklebacks: (gasterosteus spp.) Law, Tara 1994

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BIOMECHANICAL ASSESSMENT OF ADAPTIVE RADIATION IN THREESPINE STICKLEBACKS (Gasterosteus spp.) by TARA LAW B.Sc., The University of British Columbia, 1989  A THESIS SUBMI El ED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE  in THE FACULTY OF GRADUATE STUDIES (Department of Zoology)  We accept this thesis as conforming  THE UNIVERSITY OF BRITISH COLUMBIA April 1994 © Tara Law, 1994  requirements for an advanced in presenting this thesis in partial fulfilment of the the Library shall make it degree at the University of British Columbia, I agree that that permission for extensive freely available for reference and study. 1 further agree granted by the head of my copying of this thesis for scholarly purposes may be is understood that copying or department or by his or her representatives. it allowed without my written publication of this thesis for financial gain shall not be permission.  ture)  (Signa  /o. ,‘  Department of  The University of British Columbia Vancouver, Canada Date  DE-6 (2/88)  2  .  /7  V  ii ABSTRACT This study compares the morphological characteristics and swimming performances of a sympatric species pair of threespine stickleback in order to gain an understanding of the processes involved in their divergence. The fishes are young (13,000 years old), morphologically distinct, and inhabit different niches in the lake (Paxton Lake, Texada Island, British Columbia). Experiments were conducted to compare the steady swimming and escape fast-start performances of these fishes. I tested predictions of two hypotheses: 1) Selection has acted on the steady swimming ability of limnetics, and therefore I predicted that limnetics have greater steady swimming performance than benthics. 2) The specialization for steady swimming has compromised the fast-start performance of limnetics; consequently I predicted that benthics have greater fast-start performance than limnetics. As predicted, limnetics had greater steady swimming performance than benthics. The mean regression of the logarithm of fatigue time (F.T.) on swimming speed (U, in body lengths/second) for limnetics [Log (ET.) than that for benthics [Log (F.T.)  =  3.77  =  -  5.24 0.46U] was significantly higher (p <0.05) -  0.43U]. The streamlined shape (to reduce drag),  larger pectoral muscles (to provide power), and larger pectoral fin areas (to provide thrust) all contribute to the higher performance of limnetics. However, the fast-start performance of the two fishes was not significantly different for any linear parameter (pooled mean values for total fast-start: duration 0.049 s, distance 0.034 m, maximum velocity 1.10 m/s, and . With large, caudally placed fins limnetics achieved equal mIs ) maximum acceleration 133.9 2 fast-start performance to the deeper bodied benthics. The prevailing view of functional morphology in fishes is that adaptations for high performance in one swimming mode compromise those for high performance in the other swimming modes. For example, optimal characteristics for fast-starts are thought to trade-off against optimal traits for manoeuvering and steady swimming. However, both of the  iii sticklebacks studied here were capable of good manoeuverability and fast-start performance. The propulsive systems of these fish aie decoupled; consequently there is no trade-off between adaptations for these swimming modes. Limnetics achieved high performance in all three swimming categories with no compromise between good steady swimming and faststart ability. The differences in prolonged swimming performance are linked to morphological and habitat differences. I suggest that selection due to differential resource use has lead to divergence of body form and therefore of steady swimming performance. However, the results of this study also suggest that selection from predators has lead to maintenance of high performance in fast-start swimming. Predation pressure is probably similar on these fishes; consequently selection would favour traits which enhance high escape fast-start performance in both species.  iv TABLE OF CONTENTS I. Absact.ii II. List of Tables  vi  III. List of Figures  vii  IV. Acknowledgements V. Chapter 1  -  General Introduction  viii 1  VI. Chapter 2- Steady Swimming Performance A. Introduction  5  B. Materials and Methods 1. Fish Collection and Maintenance 2. Swimming Performance 3. Morphological Measurements 4. Drag Tests 5. Statistical Tests  6 7 8 10 12  C. Results 1. Swimming Performance 2. Morphological Measurements 3. Drag Tests  13 14 14  D. Discussion  15  VII. Chapter 3 Escape Fast-Start Performance -  A. Introduction  27  B. Materials and Methods 1. Fish Collection and Maintenance 2. Fast-Start Performance 3. Film Analysis 4. Morphological Measurements 5. Statistical Tests  28 28 29 31 32  C. Results 1. Fast-Start Performance 2. Kinematics 3. Morphological Measurements  32 33 34  V  D. Discussion  .35  VIII. Chapter 4- General Discussion and Conclusions  46  IX. Bibliography  50  vi LIST OF TABLES  Table I Swimming Endurance at Absolute Speeds  .20  Table II Morphological Measurements: Morphometrics  21  Table III Escape Fast-Start Performance  40  Table IV Morphological Measurements: Fin Areas and Positions of Maximum Mass and Added Mass  41  -  -  -  -  vii LIST OF FIGURES Figure 1 The Endurance of Sticklebacks  .22  Figure 2  23  -  Part A Drawings of Paxton Lake Limnetic and Benthic Threespine Sticklebacks. -  Part B Body Depth Along the Length of the Stickleback. -  Figure 3 The Drag of Sticklebacks  24  Figure 4 The Coefficient of Drag for Sticklebacks  25  Figure 5 The Endurance of a Variety of Small Fishes  26  Figure 6- The Escape Fast-Start Performance of Stickiebacks.  42  Figure 7 Use of Three Dimensional Space During Escape Fast-Starts of Sticklebacks.  43  Figure 8 Kinematics of Escape Fast-Starts of Sticklebacks.  44  Figure 9  45  -  -  -  -  -  Part A Drawings of Paxton Lake Sticklebacks. -  Part B The Distributions of the Fish’s Mass and Added Mass Along the Length of the Body -  viii  ACKNOWLEDGEMENTS  This study could not have been completed without the advice and support of many people. I would like to thank my family for providing moral and financial support. I thank my supervisor, Robert Blake, for all that he has taught me over these years. I also thank the members of my committee for support, advice, and pep talks: J. M. Gosline, J. D. McPhail, and D. Schiuter. I would especially like to thank D. Schiuter for all his help in the collection of the animals, and the design of the experiments. I thank: T. Day, T. Hatfield, M. Linden, and L. Nagel for their help with animal collection and advice on animal care, and L. Nagel for providing the drawings in Figs. 2 and 9. Thanks also go to W. Neill for providing the environmental chamber space necessary for this project, as well as identifying the calanoid copepods to species and helping with the culturing of these animals. I thank W. Milsom for providing access to computing facilities. An enormous number of people provided useful discussions on this project, in particular I would like to thank: C. Brauner, P. Domenici, M. Eymann, D. Ghan, D. Harper, S. Inglis, M. Kasapi, F. Kroon, C. Ouimet, and J. Harris. I thank R. Andrews for being both my harshest critic and my greatest supporter. I would like to dedicate this thesis to the staff of the Department of Zoology at the University of British Columbia. Without their help none of us would be able to carry on our scientific investigations.  1  CHAPTER 1  General Introduction  Although understanding the mechanisms involved in speciation is a central problem in evolutionary biology, the processes thought to be responsible for adaptive radiation are not very well understood (Schiuter 1993). Inferential studies can correctly define selective processes only if the investigation includes a knowledge of both the organism’s ecology (Clarke 1978) and a particular trait’s functional significance (Bock 1980). In addition, the processes involved can only be inferred from the study of incipient or recent species (Mayr 1978). Therefore, situations where speciation has occurred recently, and where the ecology of the animals and functional significance of their characteristics are known are ideal for investigations of the mechanisms involved in the divergence of species. The majority of studies investigating the causes of diversity among fish have concentrated on trophic morphology and its correlation with food type (Bentzen and McPhail 1984; Ehlinger and Wilson 1988; Larson 1976; Lavin and McPhail 1985, 1986; Liem 1974; McPhail 1984, 1992; Schiuter 1993, 1994; Schluter and McPhail 1992; Wainwright 1988; Werner 1977). These studies have shown that morphology and resource use are correlated (Liem 1974; Larson 1976; Lavin and McPhail 1985; Schiuter and McPhail 1992; Wainwright 1988), that morphology and resource use efficiency are correlated (Bentzen and McPhail 1984; Larson 1976; Schiuter 1993, 1994; Schluter and McPhail 1992; Werner 1977), and that resource use efficiency and growth (a fitness component) are correlated (Schiuter 1994). Factors other than the manipulation and ingestion of prey can affect the fish’s fitness. The abilities to find prey and escape predators also contribute to the fitness of an animal (Videler 1993). Success in these activities is largely determined by the fish’s swimming abilities  2 (Webb 1984a). The contribution of various features of the fish’s body to its swimming performance can be determined using a biomechanical approach (Blake 1983; Webb 1984a; Weihs and Webb 1984). The prevailing view of functional morphology in fishes is that there is mutual exclusion of optimum body characteristics for three different modes of swimming: transient (burst swimming), steady swimming (cruising), and manoeuvering (Webb 1984a). Characteristics that enhance performance in a particular swimming mode are thought to compromise performance in the others. The design elements resulting in the best transientswimming performance, such as large body depth and a large percentage of the body mass as anaerobic muscle, are costly during steady swimming, whereas characteristics such as streamlining, and a high proportion of the body’s muscle mass made up of aerobic muscle are important for steady swimming (Blake 1983; Lindsey 1978; Webb 1975). In addition, the large surface areas of the body and fins of manoeuvering specialists increase drag, which hinders steady swimming performance, and their shortened body decreases the available space for the muscle mass needed for burst swimming (Webb 1984a). Therefore, fish have been classified as being steady swimming, fast-start or manoeuvering specialists, or generalists (Webb 1984a). Generalists have good performance at more than one swimming mode but superior performance in none. To test the applicability of this model, the swimming performances of a variety of fishes with differing body designs and lifestyles have been compared (Domenici and Blake 1991; Harper and Blake 1990; Kasapi et a!. 1993). In general, these studies have compared unrelated or distantly related fishes. This study is a comparison of the body characteristics and swimming performances of closely related fishes. A sympatric species pair of threespine stickleback (Gasterosteus spp.) from Paxton Lake, Texada Island, British Columbia, was studied in order to gain an understanding of the processes involved in their divergence.  3 A number of studies have investigated the diversity of morphologies of Gasterosteus spp. in the southwestern region of British Columbia (Baumgartner et al. 1988; Bentzen and McPhail 1984; Bentzen et a!. 1984; Larson 1976; Lavin and McPhail 1985, 1986; McPhail 1984, 1992; Schiuter 1993; Schiuter and McPhail 1992). This species complex provides an opportunity to study recent divergence because all the species are endemic to coastal water systems that did not form until 13,000 years ago (Mathews et al. 1970). These studies have shown morphological differences between anadromous and stream sticklebacks (Taylor and McPhail 1986), sticklebacks from different lakes (Lavin and McPhail 1985, 1986; Schluter and McPhail 1992), and sticklebacks within the same lake (Baumgartner et al. 1988; Bentzen and McPhail 1984; Bentzen et a!. 1984; Larson 1976; McPhail 1984, 1992; Schiuter 1993; Schluter and McPhail 1992). Morphological differences are particularly pronounced between species occurring in the same lake (Schluter and McPhail 1992). The species pair found in Paxton Lake, British Columbia, was chosen for this study as an example of closely related fishes with pronounced differences in morphology. Evidence that these are a species pair and not a single polymorphic species include the observations that morphological differences are retained when fish are bred in the laboratory (Larson 1976; McPhail 1992), that hybrids are morphologically intermediate (McPhail 1992; Schluter 1993), and that the morphological and allelic frequencies between the forms have been stable for over 20 generations (McPhail 1992). The differences between the sympatric fishes are therefore thought to be genetically based and there appears to be little gene flow between the two fishes (McPhail 1992; Schluter 1993). Previous studies of this sympatric species pair have investigated spatial and trophic segregation (Larson 1976), morphological and genetic differences (McPhail 1992), trophic morphology and feeding efficiency (Schluter 1993), and feeding efficiency and growth (Schiuter 1994). The two fishes occupy different regions of the lake and have been referred to as benthic and limnetic, according to their primary habitat. Benthics live near the bottom  4  in weedy areas, and feed primarily on large insect larvae (Larson 1976; Schiuter 1993; Schluter and McPhail 1992). Limnetics form large schools in the pelagic region of the lake, and feed primarily on zooplankton (Larson 1976; Schluter 1993; Schluter and McPhail 1992). The benthic region is a spatially complex habitat where precise manoeuvering is important, whereas the pelagic region is an open habitat where steady swimming is important Here I have considered two main functions of fish swimming: cruising to locate prey (Chapter 2), and fast-starts to escape predators (Chapter 3). I tested predictions of two hypotheses: 1) Selection has acted on the steady swimming ability of limnetics and therefore I predict that limnetics will have greater steady swimming performance than benthics. 2) The specialization for steady swimming has compromised the fast-start performance of limnetics and therefore I predict that benthics will have greater fast-start performance than limnetics.  5  CHAPTER 2  Steady Swimming Performance  INTRODUCTION  The ability to swim quickly and steadily for a long time is important for fish that are pelagic (Wardle 1977). Pelagic fish feed on prey that usually have patchy distributions in an open environment, and routinely swim for prolonged periods, searching for these patches (Horwood and Cushing 1977). Pelagic fish are specialists for steady swimming and have superior performance to fish that only swim occasionally (Webb 1984a). The body design of these pelagic fish is considered to be optimal for steady swimming and includes such characteristics as streamlining to reduce drag, stiffening of the body to minimize movement of the head, and a high percentage of aerobic fibers in the body’s muscle mass (Blake 1983; Lindsey 1978; Webb 1975). Most pelagic fish swim by undulations of the body and caudal ‘fin; consequently previous studies of steady swimming performance have concentrated on such fish (e.g. Beamish 1984; Brett 1965; Taylor and McPhail 1985; Tsukamoto et a!. 1975; Tsukuyki and Williscroft 1977). Paired fin swimming is advantageous for manoeuverability at low speeds but disadvantageous for high speed, steady swimming (Blake 1983; Weihs and Webb 1984). Butterfly fish and angelfish have characteristics thought to enhance manoeuverability, but the large surface areas of the body and fins impose a high price in increased drag for steady swimming (Webb 1984a). In addition, these fish tend to have a shortened body which decreases the available space for the aerobic muscle mass needed for high speed cruising. A  6 few studies have investigated the steady swimming ability of fish which swim using pectoral fins, but these have concentrated on low speed swimming (Dom et al. 1979; Stahlberg and  Peckman 1987; Taylor and McPhail 1986; Whoriskey and Wootton 1987). This part of my investigation compares the steady swimming performances of the two species of threespine stickleback (Gasterosteus spp.) that live sympathcally in Paxton Lake. Sticklebacks use paired pectoral fins for routine locomotion, mostly by rowing (Taylor and McPhail 1986). Therefore, these fish should have good manoeuverability but poor steady swimming performance. However, many sticklebacks are anadromous, migrating great distances to breeding grounds (Wootton 1976, 1984), and others (e.g. limnetics) must swim for prolonged periods while searching for patches of planktonic prey. Limnetics live in an open water habitat and are more fusiform than benthics; therefore my hypothesis is that selection has acted to increase the steady swimming performance of limnetics but not benthics. Based on this hypothesis I have predicted that limnetics have greater endurance and experience less drag than benthics.  MATERIALS AND METHODS  Fish Collection and Maintenance Fish were collected from Paxton Lake, Texada Island, British Columbia (17-ha lake, 490  42’ 30” N, 1240 31’ 30” W) using minnow traps and dip nets. Only juvenile and adult fish  were used (i.e. no young of the year). Fish were transported to the lab where they were visually separated into the two species based on size, shape, and colour (Fig. 2 A) and placed into holding tanks.  7  Four 163 litre holding tanks were each divided into three equal sections with limestone gravel bottom cover (to maintain pH 7.8  -  8.2, similar to Paxton Lake water;  Larson 1972), plants, air stone, mini water filter, and 14 Watt full spectrum light on a natural dawn to dusk light schedule (6 am to 10 pm). The tanks were kept in an environment chamber to maintain a constant temperature of 15° ± 1°C. Holding tank water consisted of fresh, dechlorinated water and 3 % salt. Two fish of each species were placed into each section of the four holding tanks and held for one week prior to testing. During the initial week, sick or dead fish were removed, and replaced with healthy fish. All fish were individually identified by colour patterns or slight size differences and assigned a number. Fish were fed live brine shrimp nauplii, live calanoid copepods (Diaptomus oregonensis, from Paxton Lake), and either previously frozen adult brine shrimp or blood worms, once per day during the initial week.  Swimming Performance Feeding ceased one day prior to testing to ensure a post-absorptive state (Niimi and Beamish 1974). The experiments were carried out at 15° ± 1°C in a 12 liter flow tank (working section 10 cm x 60 cm x 10 cm) with an adjustable speed controlled propeller motor (Cole-Parmer model 4555-3). Water velocity was monitored with a small velocity probe and meter (Nixon Streamflo 422, ± 1 cmfs). Water (pretreated for a minimum of three days with limestone, 3  %o  salt, and aeration) was replaced daily to ensure similar conditions  as in the holding tanks. The flow was smoothed by a straw grid at the upstream end of the working section. A downstream screen prevented the fish from being swept into the propeller. For each trial the water speed was set, then the selected fish was added. The observer sat close to the tank with a stopwatch and measured the time to fatigue, or up to an arbitrarily  8 defined cutoff time of sixty minutes, at which time the fish was removed and returned to the holding tanks. Fatigue time was defined as the time until a fish ceased swimming and fell  back against the downstream screen. Every fish (benthic n  =  10, limnetic n  =  9) was tested once each at five speeds: 27.0,  36.0, 40.5,44.5, and 53.5 cm/s, and allowed 48 hours rest between trials. The regression of fatigue time on swimming speed was calculated for every fish and the mean slopes and intercepts of the two species were compared. Trials where the fish were still swimming at the cut off time of 60 minutes were included as this gave conservative estimates of the regression slopes. Hoar and Randall (1978) define prolonged swimming as a range of speeds between burst and sustained swimming, where the swimming period lasts between 15 seconds and 200 minutes and if maintained will end in fatigue. For both limnetics and benthics the speeds were chosen to allow a range of speeds to be tested that were within this definition.  Morphological Measurements Fish were killed by an overdose of MS222, dried externally with a paper towel, and weighed with an analytical balance (Mettler Scale model PK300 ± 0.001 g). Standard lengths (L  =  tip of rostrum to end of caudal peduncle) were measured with vernier calipers (±  0.005 cm). The centre of mass (CM) of a fish was determined by suspending the fish from the mouth and marking the vertical line of gravity and repeating this procedure for suspension from the cloaca. The CM was the point where the two lines cross. The CM as a proportion of the length was the distance along the straight body from the tip of the rostrum to the CM, and the distance from the fishes dorsal surface to the CM was the CM as a proportion of body depth. The body depth at the CM was measured with vernier calipers (±0.005 cm).  9  To determine the position of maximum body depth, depth was measured at intervals of 10% of total length (0.1L) from the tip of rostrum to the trailing edge of caudal fin, while the fish was submerged in water in a petri dish to ensure full extension of the fins. Pectoral fin areas were measured by painting the fins with methylene blue and blotting the splayed fins onto paper. The resulting fin prints were cut Out and weighed (Mettler model M3 ± 0.001 mg). The mass was then converted to area using a regression obtained by weighing known areas of the same paper. Surface area (Sw) was measured by wrapping the body of the fish with plastic wrap (Glad Cling Wrap), weighing the resultant plastic piece, and converting the weight to area (Varley 1989), as done for the fin areas. In the calculation of fin areas as percentages of total surface area, all surfaces of the fins were included, and the fins were considered to have zero thickness. The right pectoral muscles, both abductor and adductor, easily distinguished from surrounding muscle by their red colour, were dissected out of the fish and weighed together. There is a significant difference in the size of the two species (McPhail 1992), and body proportions are size dependent; therefore, morphological measurements were corrected for size using a regression method for adjusting treatment means (Steel and Tome 1980). This adjustment uses the linear regressions of the log of each variable on the log of standard length. The adjustment equation is: A  —  (1)  YjJk=Yjk-Bjk(L-5.O) where  is the adjusted measurement of the  population,  jk  is the sample mean of the  jth  jth  variable for the  th 1  individual in the kth  variable in the kth population, BJk is the  coefficient of allometry for the jth variable on standard length for the kth population, and Lik 5.0 is the standard length of the  jth  -  individual minus the standardizing size. In Gasterosteus it  is conventional to use 5.0 cm as a standardizing size for comparison (Hagen and Gilbertson 1973; Lavin and McPhail 1985; McPhail 1983). In addition, 5.0 cm is approximately half-  10 way between the mean benthic length (5.4 cm) and the mean limnetic length (4.5 cm). Therefore, the adjustment affects the two species an equal amount. Submerged weight was measured with the fish first squeezed under the water to remove air bubbles, and then weighed with an electronic balance equipped with an adaptor which suspended the fish in the fluid (Mettler PK300 with manufacturer’s submerged weight adapter ± 0.001 g). The density of the fish  (p’)  was calculated using (2)  Ws=Wa(1P/P’) (Gal and Blake 1987) where W is the submerged weight, Wa the weight of the fish in air, and p is the water density. Fish density was calculated as: =  (3)  _p_ WaWs  The sex of the fish and the presence of any external or internal parasites were recorded. Fish that were obviously gravid or parasitized were not used.  Drag Tests Teminal velocity estimates were obtained by dropping dead fish down a glass column (30 x 32 x 120 cm) filled with water at room temperature, 20°C (water density , kinematic viscosity 2 0.998 glcm  =  0.01004 cm /s, Vogel 1981). The rigid-body assumption 2  for dead-drag drop tank tests does not apply to fish that swim using body undulations because of additional pressure and friction drag associated with repeated bending, but fish that swim using paired fins (e.g. sticklebacks) hold their body rigid. Therefore, dead-drag measurements can be assumed to give a good indication of true swimming drag (Blake 1983). To obtain a relationship between drag and velocity for every fish, each fish was dropped at a number of different weights. Submerged weights of the fish were increased by  11 inserting small lead balls through the mouth without extending the pharyngeal pouch. Submerged weights were measured as described above. For each fish at a given weight, three  separate trials were conducted and the results averaged. To achieve a vertical descent, a dart flight (wetted surface area  =  20.11 cm ) was 2  attached to the fish on the end of a shaft made from thin wire (diameter 0.07 cm) which was inserted through the caudal peduncle, parallel to the spinal column. The dart flight was attached 10 cm from the trailing edge of the fish’s caudal fin to reduce interference. In addition, the pectoral, dorsal, and anal fins were removed, flush with the body, to eliminate fin flutter, and to ensure a vertical descent (Blake 1983; Varley 1989). Two lines on the outside of the column (55.5 cm apart) marked start and end for timing. The column was filmed with a video camera (Panasonic CCTV camera model WV BL600) connected to a 60 frame/second VHS recorder (J.V.C. video cassette recorder model B2-3200U). A 1/100 second counter (Panasonic model WJ-810) fed directly into the recorder  as part of the image. The time used in the calculation of terminal velocity was the difference between the counter time when the dart flight passed the top mark line and the counter time when the flight crossed the bottom mark line. Terminal velocity was always reached prior to the dart flight crossing the start line. A drag-terminal velocity calibration curve for the dart flight and shaft was also determined. Submerged weights were increased by rolling thin sheets of lead around the leading end of the flight shaft. The regression of drag on terminal velocity for the fish was calculated by subtracting the curve for the flight from the curve for the flight attached to the fish. At terminal velocity, the submerged weight of the fish is equal to the drag force, D: W  =  D  =  CD 2 O.5PSWU  (4)  (Gal and Blake 1987) where U is the velocity, S is wetted surface area, and CD is the drag coefficient. Therefore, the drag coefficient can be calculated as:  12 CDt  2D pSU 2  (5)  Reynolds number, Re, can be calculated from: Re=LII  (6)  1)  (Vogel 1981) where L is length, U is velocity and 1.) is the kinematic viscosity of the fluid. To remove the effect of variation in terminal velocities between fish, the drag at 10 velocities (.250, .270, .300, .360, .405, .445, .490, .535, and .600 m/s) was calculated for each fish using the regression equation for drag on terminal velocity for that particular fish. These drag data were then corrected for size using the adjustment technique described above. Drag was then compared between the fish at each velocity and the mean regression for drag on velocity calculated for each species. Coefficients of drag were calculated using the size adjusted drag values. Therefore, direct comparisons of coefficients of drag at each Reynolds number were possible.  Statistical Tests All data were compared using t-tests except the position of maximum body depth along the length of the fish which was compared using a Mann-Whitney U test. Percentage and proportion data were arcsin-square root transformed before testing with t-tests. All null hypotheses were rejected at p <0.05 and all means are presented ± 2 S.E.  13  RESULTS  Swimming Performance Both fishes primarily used pectoral fin locomotion, although occasional caudal fin thrusts to maintain position at higher speeds were observed. Limnetics collapsed their dorsal and anal fins, raising them only during quick bursts, whereas benthics had raised fins continuously. There was no difference in swimming performance between males and females within a species (p > 0.05), so the data for a species were pooled. All limnetics (n  =  9), and all but one benthic (total n  =  10), were able to swim for the  entire 60 minute thai period at 27 cm/s. Limnetics swam for longer at all other speeds than the benthics (Table I). The convention is to show endurance data as the logarithm of fatigue time compared to speed in body lengths/second, L/s (Brett 1965). Using this convention, limnetics showed superior performance to benthics (Fig. 1). The regressions of fatigue time on swimming speed for all fish were significant (p <0.05), and the r 2 values ranged from 0.87  -  0.99 with the mean for both fishes at 0.95. The mean intercept of the regression for  limnetics (5.24 ± 1.18) was significantly (p  <  0.05) higher than that for benthics (3.77 ±  0.44). Although the slopes were not significantly different (benthic =  -0.43 ± 0.06, limnetic  -0.46 ± 0.12), the limnetic slope was slightly steeper than the benthic slope which caused  convergence of the regression lines at higher speeds. The benthic mean regression equation was Log (F.T.)  =  3.77 0.43U -  (7)  and the limnetic mean regression was Log (F.T.)  =  5.24 0.46U. -  (8)  14  Where F.T. is fatigue time (minutes) and U is swimming speed (body lengths/second). There was no allometric effect on endurance for benthics or limnetics (p  >  0.05).  Morphological Measurements Although benthics are larger, heavier, and deeper bodied than limnetics, the fish whole body density and the pectoral muscle mass for the two species were not significantly different (Table II). The pectoral fin area as a percentage of the total surface area was significantly larger (p <0.05) for limnetics 12.2% ± 0.03%) than benthics (7.8% ± 0.02%). Pectoral fin muscle mass as a percentage of the total body mass was also greater for limnetics (3.0% ± 0.005%) than benthics (1.3% ± 0.004%). The position of maximum depth for the two fish also differed. Benthics were deepest at 0.3L, and limnetics at 0.6L, the region where the dorsal and anal fins both contribute to depth (Fig. 2). Size corrected measurements showed large differences between the two fishes. Although benthics have greater mass and surface area than limnetics, their pectoral muscle mass and pectoral fin area were significantly smaller. There was no relationship (p  >  0.05)  between density and size for either of these fishes.  Drag Tests The size corrected drag was significantly higher (p <0.05) for benthics than limnetics at all speeds (Fig. 3). Drag coefficients for benthics were also greater than those for limnetics at all Reynolds numbers (Fig. 4).  15  DISCUSSION  As predicted, limnetics had superior steady swimming performance compared to benthics. The endurance of limnetics ranged from 1.5 to 7.5 times that of benthics. Although limnetics had greater performance at all speeds, the difference between the fishes was less at higher speeds. The steady swimming ability of limnetics relates to the lifestyle of these fish. Limnetics are open water fish that feed primarily on calanoid copepod zooplankton (Schiuter 1993). Zooplankton populations are typically found in patches throughout lakes (Richerson et al. 1977; Steele 1977). Thus, limnetics must travel relatively large distances in search of prey and therefore must have good steady swimming ability. The results of the morphological measurements indicate that there is significant differentiation with respect to morphology. This differentiation was characterized by both allometric and shape variation. Benthics are larger, heavier, more robust fish, with larger surface areas. Limnetics are smaller, more fusiform fish, with smaller surface areas. Size corrected measurements showed that the pectoral fin area and pectoral muscle mass of the smaller fish (limnetic) were 2 and 3 times greater, respectively, than for the larger fish (benthic). The morphological characteristics considered to be advantageous for steady swimming include streamlining to minimize drag, stiffening of the body to minimize recoil, and a high percentage of the body’s mass made up of aerobic muscle (Webb 1984a). There are differences between the two fishes for all of these characteristics. Drop tank tests showed that the streamlined shape of limnetics results in lower drag. The size corrected drag was 2 times less for the limnetic fish than for the benthic fish. In  16 addition to having a streamlined body to reduce drag, limnetics collapse their fins, thereby reducing fin flutter and surface area. The position of maximum body depth for limnetics is far back on the body (Table II and Fig. 2), and the depth is mostly due to the dorsal and anal fin heights. Thus, by collapsing the fins limnetics reduce their maximum body depth, thereby reducing drag. Benthics, however, do not gain the advantage of decreasing maximum body depth by collapsing their fms because the position of maximum depth for these fish is due entirely to body depth. Therefore, collapsing the fins would not significantly reduce the drag experienced by benthics. Limnetics have a pelvic girdle and lateral plates which may increase stiffness for prolonged swimming. The pelvic girdle is absent in the benthics and the number of lateral plates is greatly reduced (McPhail 1992). Although pectoral fin swimmers do not bend their bodies while swimming, if muscular effort is required to maintain a rigid body, the greater body stiffness of limnetics would enhance steady swimming by reducing the muscular energy needed to hold the body rigid. Thus the lower body stiffness of benthics may reduce their steady swimming performance. The pectoral muscles of the sticklebacks make up a relatively large percentage of their total body mass, an advantage for endurance during prolonged swimming. Limnetics have larger pectoral muscles, and a greater percentage of their body mass as pectoral muscle mass than benthics. The relative amount of aerobic muscle in the body is an important characteristic for swimming performance (Webb 1984a). The pectoral muscles dissected from the sticklebacks were red in colour and are likely composed of aerobic muscle fibers. Boddeke et al. (1959) found that the pectoral muscles of the River Bullhead, a labriform swimmer, were entirely made up of red aerobic fibres. During the routine, steady swimming of the sticklebacks, the pectoral muscles were used almost exclusively. Therefore, this activity should be aerobic. However, Luiker and Stevens (1992) found white fibers mixed with the red fibers in the pectoral muscles of the sunfish (Lepomis gibbosus). The prolonged  17 swimming of sticklebacks may be entirely aerobic, or partially anaerobic. A complete histochemical analysis of the pectoral muscles of these fishes is necessary to determine the extent of the aerobic contribution to prolonged swimming. Wardle (1977) considered fast sustained cruising only an advantage for pelagic feeders. Such steady swimming ability is a significant determinate of the feeding success of these fish (Videler 1993). The streamlined body of the limnetic reduces the drag experienced, and the larger pectoral fins and pectoral muscles increase the thrust per stroke, thereby enhancing steady swimming performance. Benthics, however, live in a complex vegetated habitat where they feed by hovering above a prey item (e.g. insect larvae) on, or in, the sediment, and swim slowly closer to suck in a mouthful of substrate and prey (Anker 1978). Finding prey requires careful examination of the substrate rather than searching large areas by swimming. Therefore, superior steady swimming performance is not necessary for the feeding success of benthics. There are difficulties in comparing the swimming performance results of this study to others because the majority of researchers have determined critical speed, rather than endurance at a range of speeds. Farlinger and Beamish (1977) have shown that the methods used to determine critical speed, in particular the time increments for increasing speed, greatly affect maximum endurance. At the end of step tests, fish swim rapidly and probably anaerobically. Whereas, during endurance tests fish swim relatively slowly and most probably aerobically (Kolok 1992). Step tests pre-exhaust fish to anaerobic levels; therefore, endurance tests provide a more accurate measure of a fish’s ability to swim for a length of time at a certain speed (Kolok 1992). Step-tests to determine critical speeds involve prior partial fatigue of the fish, before the test velocity is reached. Consequently, these tests tend to give underestimates of the endurance performance of fish. In addition, endurance trials at a variety of speeds allow for comparisons of different fishes at several speeds, as well as an indication of the differences within one fish type at a range of speeds. The use in this study  18 of endurance trials at a variety of speeds for each fish showed that limnetics had greater endurance than benthics over the entire range of prolonged swimming speeds (Fig. 1). Figure 5 shows the steady swimming performance of a variety of fishes. All the fishes shown here are between three and ten cm in length. Thus, the confounding factors of allometric effects are reduced. Both fishes which use body/caudal fin undulations, and fishes which use pectoral fins for locomotion are shown. Since the two modes of swimming are different in movement, muscle use, and drag augmentation, it is difficult to interpret the exact meaning of comparative results. Comparisons with other pectoral fin swimmers is perhaps more appropriate. In general, benthic steady swimming performance could be considered average to poor, and limnetic performance considered superior to other fishes, both pectoral and caudal fin swimmers. Several researchers have investigated the steady swimming performance of Gasterosteus spp. from a variety of different locales (Stahlberg and Peckman 1987; Taylor and McPhail 1986; Whoriskey and Wootton 1987). Taylor and McPhail (1986) studied two different morph types of threespine sticklebacks and found that the streamlined anadromous fish had longer fatigue times than the more robust stream fish. Although their results were in the same direction as the results of this study, the swimming performance of the limnetics was greater than that for the anadromous sticklebacks (Fig. 5). The performance of stream sticklebacks studied by Stahlberg and Peckman (1987) was lower than that of benthics (Fig. 5). However, the stream sticklebacks studied by Whoriskey and Wootton (1987) had an intermediate performance between that for limnetics and benthics (Fig. 5). In general, it appears that the limnetics are at the extreme in the stickleback gradation of morphologies for superiority in steady swimming performance and that the benthics are towards the extreme for poor performance. The superior prolonged swimming performance of limnetics compared to benthics can be explained by their morphological differences. There was a 1.5 to 7.5 times difference  19 in swimming endurance, and, although probably not directly additive, the differences in drag (limnetics 2 X less), pectoral muscle mass (limnetics 3 X more), and pectoral fin area (limnetics 2 X greater) more than account for the greater performance of limnetics. The streamlined shape reduces drag, the large pectoral muscles increase the power available for thrust, and the large pectoral fins increase the area generating thrust thereby increasing the performance of limnetics. These results support my hypothesis that divergent selection has led to a high steady swimming performance of limnetics compared to benthics.  TABLE I Swimming Endurance at Absolute Speeds  20  -  Swimming Endurance in Minutes (±2 S.E. Benthic  Limnetic  36.0  12.58 (11.8)  44.46 (15.6)  *  40.5  3.15 (1.9)  16.45 (12.4)  *  44.5  1.73 (1.1)  13.16 (1.4)  *  53.5  0.82 (0.2)  1.17 (0.5)  *  Speed (cmls’  * significantly different at <0.05 p Benthic n  =  10 Limnetic n =9  *  4.51 (0.16) 1.072 (0.02 1) 0.32 (0.03) 10.41 (0.84) 0.016 (0.003) 0.88 (0.06) 0.55D (0.06)  0.45L (0.04) 0.6L 1.006 (0.005) 0.41 (0.03) 10.51 (0.04) 0.034(0.006)  5.41 (0.22)  1.063 (0.011) 0.42 (0.06) 21.38 (2.9) 0.019 (0.004) 1.09 (0.04) 0.56D (0.04) 0.44L (0.02) 0.3L 1.758 (0.037) 0.26 (0.02) 20.87 (0.08) 0.010 (0.003)  Length (cm)  ) 3 Density (glcm  ) 2 Pectoral Fin Area (cm  ) 2 Total Surface Area (cm  Pectoral Muscle Mass (g)  Depth at Centre of Mass (cm)  Position of Centre of Mass Along Depth  Position of Centre of Mass Along Length  Position of Maximum Depth Along Length  Size Corrected Mass (g)  ) 2 Size Corrected Pectoral Fin Area (cm  ) 2 Size Corrected Total Surface Area (cm  Size Corrected Pectoral Muscle Mass (g)  Benthics n = 10  Limnetics n =  10  * significantly different at p <0.05  *  *  * *  *  0.991 (0.16)  1.904 (0.34)  Mass (g)  *  *  *  *  Limnetic  Benthic  Parameter  TABLE TI- Morphological Measurements: Morphometrics (±2 S.E.)  -  •  I  0 Do  •••  . .  I  .  •  I  I  .—  8  10  12  Swimming Speed (body lengths/second)  6  -  -  Figure 1 The endurance of sticklebacks. Shown are the benthic ( o ) mean regression Log (F.T.) = 3.77 .43U and the limnetic ( • ) mean regression Log (F.T.) = 5.24 .46U, where F.T. = fatigue time (minutes) and U = swimming speed (body lengths/second).  4  I  .  0  D  I  tJ  I  •  I  .  0.1  10  D  I  H  .,-  E  E  .  r-/)  100  I  14  N)  23  A  B  B enthic 1.2  0.8 0.6  0.2  0.0  0.1  0.2  0.3  0.4  0.5  0.6  0.7  0.8  0.9  Proportion of Length Figure 2. Part A Drawings of Paxton Lake limnetic and benthic threespine stickleback (modified from Schiuter 1993). Part B Body depth along the length of the stickleback. From the rostral tip (O.OL) to the trailing edge of the caudal fm (1.OL), body depth is shown for benthics ( ) and limnetics (- — —), to determine the position of maximum body depth. -  -  1.0  r  bi  -  -  -  0.30  I  —  •  0.35  •  •  •  0.45  I  Velocity (mis)  0.40  I  0•  •  0.50  I  •  •  0.55  I  -  -  -  -  )  0.60  Figure 3 The drag of sticklebacks. Shown are the regressions for benthics ( D = O.113V’ 59 and limnetic (— —) D = O.006V 1.54 over the velocity range used for endurance trials, where D = drag (Newtons) and V = velocity (m/s).  0.25  0.00 1  0.002  0.003  0.004  0.005  •  ci)  0  0  c  0.015  0.020  0.025  0.030  0.035  0.04.0  •  15000  I •  I  ..  •  20000  — —  •  I  22500  Reynolds Number  17500  -  1 •  25000  I  1  —  ,  Figure 4- The coefficient of drag for sticklebacks. Shown are the benthic mean regression ( ) Cd = Re and the limnetic mean regression (— —) Cd = 1 .42Re where Cd = coefficient of drag and Re = Reynolds number.  12500  I  ..  •  27500  1%.) (7’  ..  Cl,  -  Q  —-  I  Swimming Speed (body lengths/second)  I  I  Figure 5 The endurance of a variety of small fishes. All fishes are between 3 and 10 cm in length. Solid symbols represent fish which swim using body/caudal fm undulations and hollow symbols represent fish which swim using pectoral fms. the benthic mean regression ( Shown are the limnetic mean regression () ), stream sticklebacks ( v ) and anadromous sticklebacks ( 0 ) (Taylor and McPhail 1986), stream sticklebacks ( ) (Whoriskey and Wootton 1987), stream sticklebacks ( c ) (Stahlberg and Peckman 1987), pumpkinseed, Lepomis gibbosus ( 0 ) (Brett and Sutherland 1964), blacksmith, Chromis punctipinnus ( C> ), A ), (Dorn et a!. 1979), coho salmon, Oncorhynchus kisutch, from coastal streams ( and from interior streams ( v ) (Taylor and McPhail 1985), goldfish, Carassius carassius ( • ) (Tsukamoto et a!. 1975), pacific sardine, Sardinops sagax ( • ) (Beamish 1984), and rainbow trout, Oncorhynchus gairdneri ( • ) (Tsuyuki and Wiffiscroft 1977).  I  27 CHAPTER 3 Escape Fast-Start Performance  INTRODUCTION  Fast-starts are used by many fish to catch evasive prey or to escape from predators (Harper and Blake 1988; Rand and Lauder 1981; Webb 1984b, Webb and Skadsen 1980). Success in these behaviours, particularly predator evasion, has a direct impact on fitness (Videler 1993). Therefore, selection for characteristics which enhance fast-start performance are under intense selective pressure in fishes under high predation risk (Domenici and Blake 1991; Frith and Blake 1991; Harper and Blake 1990; Kasapi et al. 1993; Webb 1975; Weihs 1973). Investigation of the morphology and performance of fish during escape fast-starts can give an indication of the intensity of predation pressure. The ability of fish to escape predators may depend upon linear performance, such as velocity and acceleration (Domenici and Blake 1993; Harper and Blake 1988, 1990; Vinyard 1982; Webb 1976; Weihs and Webb 1984), accurate timing (Eaton and Hackett 1984), and turning ability (Howland 1974; Webb 1982). Adaptations for effective fast-start performance are thought to include a large proportion of white muscle relative to red, large caudal fin and body depth for producing thrust, and high body flexibility (Blake 1983; Webb 1984a; Weihs 1973). Most investigators have concentrated on the fast-start performance of fishes that swim using body/caudal fin undulations (Dubois et al. 1976; Eaton et al. 1977; Frith 1990: Harper and Blake 1990; Webb 1976, 1978). Specialization for median or paired fin swimming has been hypothesized to impair burst swimming performance (Webb 1984a). However, high fast-start performances by median fin swimmers has been shown in the  28 knifefish, Xenomystus nigri (Kasapi et a!. 1993), and by paired fin swimmers, in the angelfish, Pterophyllum eimekei (Domenici and Blake 1991). These fishes are laterally compressed and have large body depth and high flexibility which enables them to achieve high fast-start performance. Sticklebacks are more fusiform in shape (Fig. 2 A) and thus are expected to have poor fast-start performance compared to angelfish or knifefish. Limnetics have a streamlined body which reduces drag and aids steady swimming (Chapt. 2), but should lower thrust production during fast-starts (Blake 1983; Webb 1984a; Weihs 1973). Benthics are larger, deeper bodied fish (Chapt. 2), and thus could produce greater thrust than limnetics during fast-starts. My hypothesis is that the morphological adaptations to steady swimming in limnetics will impair their fast-start performance; therefore, benthics should have higher fast-start performance than limnetics.  MATERIALS AND METHODS  Fish Collection and Maintenance Fish were collected at the same time and kept in the same holding tanks as described in Chapter 2.  Fast-Start Performance Fish were habituated to the bright lights (3 Berkey Coloran Halide 650W bulbs)  needed for filming by turning the lights on during feeding every day for one week prior to testing. Feeding was stopped the day before testing. Nine litres of water (pretreated for a  29 minimum of three days with limestone,  %o 3  salt, and aeration) was replaced daily in the  experimental tank. Experiments were conducted at  150 ±  1 OC.  Single, previously identified fish were transferred to the experimental glass tank (24 cm X 29 cm X 14.4 cm) and allowed to habituate for one hour prior to being startled. Attached to the back and bottom of the tank were one cm square reference grids. Black paper covered the sides of the experimental tank so that the fish could not see the approaching stimulus. A mirror angled at 45° over the tank allowed the top view of the fish to be filmed. Profile view through the front of the tank, and top view from the mirror, were filmed simultaneously (Redlake Locam camera Model 51 with Sun-Dionar 16 zoom lens at 400 frames/second using Kodak 7250 colour 400 ASA tungsten high speed reversal film). The image on the film was split by a black tape line on the back, top edge of the tank. A 1 meter pole with a rubber ball on the end was struck against the side of the tank to elicit the escape response. In all escapes analyzed, fish never touched the walls of the tank. The order in which the fish were tested was altered for each set of trials and all fish were allowed at least one day rest between trials. An escape response was successfully elicited for all fish tested.  Film Analysis One fast-stan was analyzed for each fish tested. Sequences were projected (Photo optical data analyzer, Photographic Analysis Ltd. model 224A) with frame by frame advance onto a 450 mirror, and from the mirror onto a horizontal paper. The image was magnified 2.3 to 3 times. This reduced the total error (measurement  +  framing rate) to approximately ±  13% for maximum acceleration and made negligible the error for average acceleration, velocity, and distance (Harper and Blake 1989). Escape responses have been shown to be a fixed action pattern consisting of two stages, stage 1 (Si) which consists of a unilateral contraction of the axial muscles, bending  30 the fish into a C shape, followed by stage 2 (S2), a strong propulsive stroke of the tail in the opposite  direction  (Gillette 1987). A third stage in which the fish forms another curve or  coasts is possible (Webb and Blake 1985; Weihs 1973). Conventionally, studies have focused on the first two stages (Domenici and Blake 1991; Eaton and Hackett 1984; Kasapi et al. 1993; Webb 1976, 1978). Therefore, this study included only Si and S2 for analysis. The durations of Si and S2 were defined by the changes in turn direction of the head. For each escape response the number of frames analyzed included 5 frames before the stimulus (start of Si) to 5 frames after S2. For each frame a flexible ruler was used to measure the apparent length of the fish from the top view. The position of the centre of mass (CM) along the fish’s length was then calculated for that particular fish and the position marked on the paper, along with the position of the head and the end of the caudal peduncle in the top view. Using a parallel ruler, a line was drawn from the CM on the top view to the profile view. The depth of the fish at this line was measured. The position of CM along the fish’s depth was then calculated and marked on the paper. The position of CM on the straight body of the fish is conventionally used as a point of reference for analysis of escape performance (Domenici and Blake 1991; Kasapi eta!. 1993). The centre of mass, tip of head, and end of caudal peduncle for both views were recorded frame by frame. These points were later analyzed on a digitizing pad (GTCO type, 0.61 m x 0.91 m) connected to a computer (80286 AT-compatible). Data were then transferred to another 286 AT-compatible computer for further analysis. Velocity and acceleration during the two stages were derived by means of a five point moving regression (Lanczos 1956) on distance-time data. Vertical (z-axis), forward (x-axis, parallel with front glass of tank) and lateral (y-axis, parallel with the side glass of the tank) displacements of the centre of mass were combined using vector sums to express displacement in three dimensions. The displacement of the centre of mass was calculated between frames using the equation:  31 D 5 + =(x + ) 2 ° y z  (9)  (Shenk 1984) where D is the displacement of the centre of mass between the positions at subsequent frames, and x, y, and z are the displacements of the centre of mass between the same frames in the x, y, and z directions, respectively. The pitch angle was measured on the profile view as the angle between a line through the longitudinal axis of the fish and the horizontal grid on the back of the tank, parallel to the bottom of the tank. The turning angle was determined from the top view of the fish from a line through the same portion of the fish used to determine pitch and a horizontal line (bottom grid, parallel to front of tank). The pitch measured from profile views (apparent pitch, ‘y) is affected by the orientation of the fish along the y-axis and is therefore not the true pitch angle. Therefore, the instantaneous turning angle,  t,  at each frame was also measured.  The actual pitch angle, P, was then determined by: (10)  P = arctan(tanyx cost) (Kasapi et a!. 1993).  Turning radius was measured from sequence tracings of the movement of CM. Turning radius is presented as a proportion of body length.  Morphological Measurements Measurements of weight, standard length, position of CM, fin areas, and surface area were taken as described in Chapter 2. Morphological measurements were again adjusted to a standard size (5.0 cm) as described in Chapter 2. The cross-sectional depth of the body was measured with vernier calipers (± 0.005 cm) at intervals of 10% of total length (0. 1L), while the fish was submerged in water in a petri dish to ensure full extension of the fins. The fish body was then cut into ten sections of  32  equal length (0.1L), and each section was weighed (Mettler model M3 ± 0.001 mg) to determine the distribution of mass along the length of the fish’s body. Added mass (Ma), the mass of water entrained by the fish as it moves, was calculated using: (ii)  13 2 Ma0.25P1td (Blake 1983), where p is the density of water, d is the body depth of the section, and shape-dependent constant. For most fish cross-sections  13 is close to 1  13 is a  (Blake 1983).  The sex of the fish, and the presence of any external or internal parasites were recorded. Fish which were obviously gravid or parasitized were not used.  Statistical Tests All data were compared using t-tests except the positions of maximum mass and added mass along the length of the fish, which were compared using Mann-Whitney U tests. Percentage and proportion data were arcsin-square root transformed before testing with t tests. All null hypotheses were rejected at p <0.05 and all means are presented ±2 S.E.  RESULTS  Fast-Start Performance  Linear Performance All fast starts were of the double bend type (Domenici and Blake 1991) and involved the formation of a C-shape by the body of the fish (Si), followed by a contralateral bend (S2), turning the head in the opposite direction.  33 Data for both sexes within a species were pooled because comparisons of males (benthic n =4, limnetic n =9) and females (benthic n =7, limnetic n  =  3) within a species for  all parameters in Si and S2 showed no significant differences (p > 0.05). No significant differences (p  >  0.05) between limnetics (n  =  12) and benthics (n  =  11)  were found for any of the linear parameters measured (Table III, Fig. 6). In general, fish travelled for longer during Si than during S2, accelerated and travelled faster during S2 than Si. The highest recorded total distance for a fast-start was 0.06 m, the highest velocity was 1.59 m/s, and the highest acceleration was 215.59 m/s . There were no allometric effects on 2 duration, distance, velocity, or acceleration (p  >  0.05).  Although the distances travelled during escape responses were not different for the two species (Table Ill), benthics travelled in the lateral (y-axis) and forward (x-axis) directions significantly (p  <  0.05) more than in the vertical (z-axis) direction, whereas  limnetics used all three equally (Figure 7).  Kinematics Benthics had a tighter (p <0.05) turning radius for their length (T.R./L  =  0.064 ±  0.014) than did limnetics (0.087 ± 0.018). The tighter turns of the benthics are seen on tracings of body movement during escape fast-starts (Fig. 8). There was a positive correlation between fixed time average velocity and turning radii (r = 0.58, p <0.05). Pitch angles were defined as positive if the fish’s head pointed up and negative if the fish’s head pointed down. The initial pitch angle of benthics was significantly (p  <  0.05)  more positive than the pitch angles at the ends of Si and S2. There was no significant difference (p  >  0.05) between the pitch angles at the ends of Si and S2 for benthics. The  greatest change occurred during Si, where the benthic fish changed from a positive to a negative pitch angle. Although the CM of the benthics only moved in the horizontal  34 directions (lateral, y-axis and forward, x-axis) during Si and S2, the head of the benthics pitched downward during Si. Limnetics showed no significant differences (p  >  0.05)  between initial, Si, and S2 pitch angles. Benthics had a significantly more downward pitch at the end of S2 than limnetics (p <0.05), and all benthics had a downward final escape path, whereas 3 limnetics had an upward escape path (all others went down).  Morphological Measurements There was no difference between males and females within either species for any of the morphological measurements; therefore, the data for a given species were pooled. Benthics were heavier than limnetics, and their distribution of mass (Mf) along their body length differed (Fig. 9). Benthics were heaviest at 30% of total length (0.3L), the position of maximum depth, whereas limnetics were heaviest at 0.4L where the pectoral muscles are located (Table IV, Fig. 9). (p Although the size corrected added masses (Ma) for the two fishes were not significantly different (p  >  0.05), the distributions of Ma along the length of the fish’s body  did differ (Fig. 9). Benthics had the greatest Ma at 0.3L, whereas the position of maximum Ma for limnetics was at 0.6L (Table IV). The maximum Ma did not include fins for benthics, whereas the maximum Ma for limnetics was influenced by the dorsal and anal fins. Although benthics were larger fish and therefore had larger fins, in relation to total <0.05) dorsal fins (4.8% ± 0.08%) and anal fins (4.1% ±  surface area limnetics had larger 0.09%) than benthics (dorsal fin  =  4.2% ± 0.02%; anal fin  =  3.2% ± 0.03%). The percentage  of the surface area comprised of fin area for limnetics was 28.6% (± 0.14%), and for benthics it was 2 1.46% (± 0.12%).  35 When the fin areas were corrected for size differences (Table IV), limnetics had significantly (p <0.05) larger anal fins and smaller caudal fms than benthics. The dorsal fin areas were not significantly different (p  >  0.05).  DISCUSSION  Contrary to the prediction that benthics should have higher fast-start performance than limnetics, the two fishes have equal performance. This result is consistent with the probability of these fishes encountering the same predators. The major predators of sticklebacks include piscivorous fish and diving birds (Wootton 1984). Larson (1972) found cutthroat trout in Paxton Lake, and loons are present on the lake (personal observation). These predators probably have access to both habitats used by the two species. Therefore, it seems likely that limnetics and benthics are exposed to predation pressure from the same predators and thus must share the ability to escape. This study provides a comparison of two pectoral fin propulsion specialists. The results show that this specialization does not impair performance in body/caudal fin burst swimming. Harper and Blake (1990) found that pike achieve maximum accelerations of 157.8 m/s . Some median/paired fin specialists can also achieve high accelerations during 2 escape fast-starts (Domenici and Blake 1991; Kasapi et al. 1993). Angelfish, Pterophyllum eimekei, are capable of accelerating at 79.0 m/s 2 (Domenici and Blake 1991), and knifefish, Xenomystus nigri at 127.9 m/s 2 (Kasapi et a!. 1993). These fishes are thought to be specialists for both slow speed manoeuverabiity and high speed fast-starts (Domenici and Blake 1991; Kasapi et al. 1993). Both angelfish and knifefish are laterally compressed,  36 which provides a large body depth for thrust during fast-starts. The sticklebacks in this study are more fusiform in shape, and it was therefore predicted that they should have poor faststart performance. However, these sticklebacks achieve an average maximum acceleration of 133.9 m/s , and the highest recorded acceleration was 215.9 m/s 2 . Although sticklebacks are 2 paired fin specialists and are fusiform in shape, they achieve accelerations comparable with fast-start specialists. Therefore, specialization for paired fin swimming does not compromise body/caudal fm propulsion during fast-starts. The pectoral muscles and pectoral fms used for steady swimming do not interfere with, or compromise the myotomal muscles and caudal fin used during fast-starts. These two swimming modes use decoupled propulsion systems. Consequently, high performance in both these modes is not mutually exclusive (Domenici 1993; Kasapi et al. 1993). The effect of size on fish swimming performance is widely documented (Bainbridge 1959; Wardle 1975, 1977; Webb 1976, 1977). During escape responses, larger fish attain higher velocities than smaller ones. This is because fast-start durations are longer in larger fish, whereas, acceleration is size independent (Webb 1976). When considered within a fixed time, however, both distance iravelled and maximum velocity are size independent (Webb 1976). These comparisons are among fishes of very different body sizes (Bainbridge 1959; Wardle 1975; 1977; Webb 1976). In this study, the fishes were relatively similar in size. Distance travelled, velocity, and acceleration were all found to be independent of size for these sticklebacks. Weihs (1973) hypothesized that body morphology is a key determinant of maximum acceleration of fish. Morphological characteristics of pike, such as a large surface area caudally and a high percentage of body mass as muscle, are considered favourable for high thrust production during fast-starts (Webb 1984a). Harper and Blake (1990) reported that pike achieve high acceleration during fast-starts. Intraspecific comparisons of fast-start performance for coho salmon (Taylor and McPhail 1985) and threespine stickleback (Taylor  37 and McPhail 1986) showed that fish with greater body depth and caudal fin depth are capable of greater maximum and average velocities. The caudally placed anal and dorsal fins of pike increase fast-start performance (Frith and Blake 1991). Thrust from the caudal fm and the body section which contains the dorsal and anal fins account for  >  90% of total thrust (Frith and Blake 1991). The combination of  higher velocities and angles, and larger depths in these sections all contribute to higher thrust. The posterior placement of dorsal and anal fins in pike contributes 26% of total thrust (Frith 1990). The fins increase the depth of section and therefore the added mass, and also generate lift forces (Weihs 1973). Webb (1978) found that for trout, caudally placed dorsal and anal fins contribute approximately 27% to total thrust. In addition, Webb et al. (1992) found that the low power produced by the caudal fin of the gar was compensated for by the median fins, which were caudally positioned. The dorsal fm of limnetic sticklebacks is placed further back on the body, directly above the anal fin and the anal fin surface area is enlarged in comparison to benthics. This ,  increases the body depth for limnetics and therefore increases added mass. The position of greatest added mass for limnetics is at 0.6L, where the depth is due to the dorsal and anal fin heights. The limnetic’s enlarged anal fin and caudally placed dorsal fin increase added mass where the majority of thrust is produced, thereby enhancing fast-start performance. Among fishes, depth is often enhanced to increase the added mass associated with acceleration reaction propulsion forces (Domenici and Blake 1991; Kasapi et al. 1993; Weihs 1989). Fins are more effective structures for increasing added mass than is body depth (Weihs 1989). This is because fins do not greatly increase mass which can hinder fast-start performance (deBuffrénil et al. 1985; Webb and deBuffrénil 1990; Webb and Skadsen 1980), but do increase added mass which benefits performance (Weihs 1989). Limnetics achieve a high fast-start performance by having large, caudally placed fins, and benthics achieve the same performance by having large body depth.  38 It has been suggested that turning radius is a relevant parameter in predator-prey interactions (Howland 1974; Webb 1976; Weihs and Webb 1984). Transient swimming performance has been defined as the ratio of the minimum turning radius of the center of mass to the length of the body (Webb 1984a). The smaller the ratio, the better the performance (Webb 1984a). Domenici and Blake (1991) found that angelfish had a turning radius to body length ratio (T.R.JL) of 0.065 indicating a very flexible body and high faststart performance. Benthics have a smaller T.R.IL (0.064) than limnetics (0.087), indicating greater flexibility than limnetics during fast-starts. A low value of turning radius is beneficial in complex environments such as the benthic region of the lake. However, in the open water column a tight turning radius would not be as important as the ability to move swiftly away from a predator. There is a trade-off between average escape velocity and the tightness of the turning radius for these sticklebacks, suggesting that some fish elude predators by achieving high velocities and others by changing direction sharply. Active defenses, such as acceleration and speed are reduced in those species with passive defense mechanisms, such as camouflage and armor (Eaton et at. 1977; Webb et at. 1992). Passive defence such as armor may decrease the importance of speed in fleeing for cover (Webb et a!. 1992). The sticklebacks have an elaborate defensive armor that has been linked to predation pressure (Gross 1978; Hagen and Gilbertson 1973; Reimchen 1980; Reist 1980a, 1980b). Therefore, these fishes might be expected to have reduced fast-start performance. That they have such high performance is interesting. Perhaps the damage inflicted during an encounter with a predator, even though the fish may escape, is disadvantageous to the fitness of the fish. Therefore, the ability to avoid such encounters may be under selection. Another possibility is that more than one predator is having an effect on the evolution of these fishes. One predator may be deterred by the presence of spines while another is not. Therefore, the sticklebacks would need both the presence of spines and the ability to escape quickly to successfully avoid both predators.  39 Morphological responses to differential predation pressure have been suggested by various researchers (Larson 1976; McPhail 1977; Moodie and Reimchen 1976; Reimchen 1980; Reist 1980a, 1980b). Burst swimming performance appears to be directly related to the ability to evade predators (Taylor and McPhail 1985; Webb 1981; Webb and Corolla 1981), and body shape is an important variable in defining levels of evasion. Bronmark and Miner (1992) showed that a predator can induce a phenotypical change in body morphology, specifically an increase in body depth to avoid gape limited predators. Fish specialized for manoeuvering have large body depth (Webb 1990). Benthics, which live in the complex habitat of the littoral zone, are deeper bodied than the pelagic limnetics, possibly to aid in manoeuverability. The number and length of spines is greater for limnetics than benthics (McPhail 1992). Therefore, benthics may have deeper bodies to avoid gape limited predators and increase manoeuverability, whereas limnetics have numerous, large spines to repel predators and a slender shape to reduce drag during steady swimming. With large, caudally placed fins limnetics have achieved the same thrust capabilities for fast-starts as benthics. These results suggest directional selection towards high escape fast-start performance for both species. Maintenance of high performance in these fishes is consistent with the likelihood of encounters with the same predators.  40  Table ifi Escape Fast-Start Performance (±2 S.E.) -  average acceleration (m/s)  duration (s)  distance (m)  average velocity (mis)  maximum velocity (mis)  maximum acceleration (m/s2)  Benthic  .029 (.004)  .017 (.003)  .54 (.06)  .79 (.11)  4.94 (9.78)  96.45 (24.39)  Limnetic  .027 (.003)  .018 (.003)  .60 (.06)  .88 (.09)  4.01 (9.58  92.75 (23.98)  Pooled  .028 (.003)  .017 (.002)  .57 (.04)  .84 (.07)  4.46 (6.69)  94.52 (16.73)  .021 (.008)  .017 (.006)  (.15)  1.07 (.18)  15.19 (13.08)  121.13 (24.12)  Limnetic  .021 (.003)  .017 (.004)  .86 (.18)  1.06 (.18)  19.04 (9.72)  127.99 (28.70)  Pooled  .021 (.004)  .017 (.003)  .84 (.12)  1.07 (.13)  17.20 (7.91)  124.71 (18.53)  STAGE 1  STAGE 2 Benthic  TOTAL (Si  +  .81  S2)  Benthic  .051 (.008)  .034 (.007)  .66 (.07)  1.10 (.17)  9.38 (7.16)  127.93 (24.31)  Limnetic  .048 (.004)  .034 (.006)  .70 (.10)  1.09 (.16)  10.09 (6.77)  139.41 (22.33)  Pooled  .049 (.004)  .034 (.004)  .68 (.06)  1.10 (.12)  9.75 (4.81)  133.92 (16.27)  .018 (.002)  .56 (.07)  .86 (.12)  8.61 (9.92)  101.07 (21.32)  .020 (.002)  .61 (.08)  .93 (.12)  7.74 (10.68)  101.19 (18.94)  .019 (.002)  .59 (.05)  .89  8.16  (.09)  (7.15)  101.13 (13.87)  FIXED TIME (0.03 s) Benthic  Limnetic  Pooled  Comparisons of all parameters not significant, p > 0.05 Benthic n = 11 Limnetic n 12  0.78 (0.08) 0.3L 0.3L 0.18 (0.16) 0.27 (0.06)  0.64 (0.05)  Caudal Fin Area (cm ) 2  Position of Maximum Mass Along Length  Position of Maximum Added Mass Along Length  Size Corrected Anal Fin Area (cm ) 2  Size Corrected Dorsal Fin Area (cm ) 2  Size Corrected Caudal Fin Area (cm ) 2  Benthic n  =  10 Limnetic n 10  0.44(0.05)  Dorsal Fin Area (cm ) 2  =  0.34 (0.05)  Anal Fin Area (cm ) 2  * significant at <0.05 p  Benthic  Parameter  -  0.53 (0.05)  0.34 (0.03)  0.38 (0.05)  0.6L  0.4L  0.39 (0.05)  0.25 (0.03)  0.22(0.04)  Limnetic  *  *  *  *  *  *  *  Table IV Morphological Measurements: Fin Areas and Positions of Maximum Mass and Added Mass (±2 S.E.)  Benthic  Limnetic  42  0.04 0.06  I  0.05 0.04 0.03 0.02 0.01  0.03  0.02  0.01  1.25  0.8  1.00  0.6  0.75 0.4 0.50 0.2  0.25  150  150  100  100  50 0  50  0  0  0 -50  C) C)  -50 -100  -100 -150  0.00 0.01 0.02 0.03 0.04 0.05 0.06 0.07  0.00 0.01 0.02 0.03 0.04 0.05 0.06 0.07  Time (s)  Time (s)  Figure 6 The escape fast-start performance of sticklebacks. Shown are the distance travelled, velocity and acceleration over time. The stacked graphs on the left are for a limnetic, and those on the right for a benthic. -  rd)  •  C)  —  _-4  -  0.01  —/  I-..  .,  I  —  0.02  —  I-’  Time (s)  0.03  I  /  /  I--, /  I,  /7  0.04  I  yr  0.05  “  If  1,  0.01  0.02  /  0.03  —  /  Time (s)  ---..  —  /  /  /  I  /  /  0.04  /  /  /  /  0.05  0.005  0.010  0.015  0.020  0.025  0.030  0.06  Figure 7- The use of three dimensional space during escape fast-starts of sticklebacks. Shown are the distances travelled over time in the forward direction, ( ), lateral (- — and vertical (- - —-) directions for a limnetic (left) and a benthic (right) threespine stickleback.  0.00  0.005  0.010  0.015  0.020  0.025  0.030  •i:5  C)  — —  w  -  Limnetic  10  24  26  12  28  F  Benthic  6  2  FigureS Kinematics of escape fast-starts for sticklebacks. Tracings, magnified I .5X, of the movement of a limnetic (left) and a benthic (nght) threespine stickleback during fast-start escapes. Arrowheads represent the head of the fish, and filled circles represent the centre of mass. Numbers indicate sequential tracings arid are at O.005s intervals.  18  16  6  42  45  A  B Benthic 0.8 C,,  0.6 1)  0.4 0.2  0.1  0.0  0.2  0.3  0.4  0.5  0.6  0.7  0.8  0.9  Proportion of Length Figure 9. Part A Drawings of Paxton Lake limnetic and benthic threespine stickleback (modified from Schiuter 1993). Part B The distribution of mass and added mass along the length of the fish’s body. The distribution of mass for benthics ( ) and limnetics (--- — -), and the distribution of added mass for benthics ) and limnetics (- - — -) are shown to determine the positions of maximum mass and maximum added mass for these fishes. -  -  —  1.0  46 CHAPTER 4  General Discussion and Conclusions  Webb (1984a) classified fish swimming styles into three broad categories: steady swimming (cruising), transient swimming (fast-starts), and manoeuvering. He argued that specialist fish which excel in one of these categories sacrifice performance in the others, while generalist fish perform moderately well in all of these swimming modes but have superior performance in none (Webb 1984a). Optimal morphological characteristics for one particular swimming function are thought to interfere or trade-off with the others. However, both of the sticklebacks of this study were capable of superior manoeuverability and faststart performance. Accelerating and manoeuvering imply axial locomotion and paired fin locomotion, respectively. These systems are decoupled; the propulsors for paired fin swimming do not impair those for fast-starts (Domenici 1993; Kasapi et al. 1993). The pectoral muscles and fins used for paired fin manoeuvering are separate from the myotomal muscles and body/caudal fm sections used for fast-starts. Therefore, there is no compromise between adaptations for manoeuverability and burst swimming. In addition, manoeuvering specialists can vary greatly in overall body form and still maintain high hydromechanical efficiency and thrust, whereas specialists for body/caudal fin propulsion are constrained to a few optimal designs (Blake 1994, in prep.). Limnetics achieved high performance in all three swimming categories. These fish have a streamlined body to reduce drag during steady swimming, large pectoral fins and pectoral muscles for steady swimming and manocuvering, and large, caudally placed fins for fast-starts. This is the first time a fish has been shown to excel in all three swimming categories. The compromise between good steady swimming and fast-start ability is avoided  47 with large, caudally placed fins to increase depth for fast-starts on an otherwise streamlined body. Movement through water is energetically expensive and organisms must trade-off the costs of locomotion with the benefits of the behaviour, such as encountering prey (Ware 1978). Foraging models assume that surplus power or net energy gain per unit time is maximized, and yet the cost of locomotion is often ignored (Ware 1978, 1982). A relatively large proportion of the daily energy budget of fishes is allocated to swimming (Videler 1993). Parrotfish spend 50% of their waking time swimming (Videler 1993) and pike spend approximately 20% (Lucas et al. 1991). Therefore, a large fraction of the energy budget of fish is required to fuel locomotion. Characteristics which decrease the cost of locomotion would make available surplus energy for reproduction and thereby enhance fitness (Blake 1983). Therefore, traits which decrease locomotor costs, such as streamlining to reduce drag, are under selective pressure. Several studies have shown that swimming performance and growth (a fitness component) are linked (Davison and Goldspink 1977; East and Magnan 1987; Greer Walker and Emerson 1978; Koch and Wieser 1983). East and Magnan (1987) found a negative relationship between swimming speed and growth for brook char (Salvelinus fontinalis). Experiments with Salmo trutta (Davison and Goldspink 1977) and with Oncorhychus mykiss (Greer Walker and Emerson 1978) showed a similar negative relationship between growth and swimming activity. Growth has many positive fitness consequences in fish (Schiuter 1994), such as higher overwinter survival (Conover 1992; Shuter and Post 1990), higher fecundity (Bagenal 1978; Schluter 1994), and earlier breeding (Schultz et al. 1991). In addition to locomotion and body growth relationships, gonadal growth and swimming activity have been shown to be correlated (Koch and Weiser 1983). Koch and Wieser (1983) found that while gonadal growth was occurring, swimming activity was reduced, indicating a trade-off between energy for swimming and energy for gonad synthesis. These results  48 suggest that swimming performance influences the fimess of fishes. Therefore, the characteristics that enhance performance are probably under selective pressure. How body features affect the cost of locomotion is fundamental to biomechanical studies (Blake 1983; Frith and Blake 1991; Harper and Blake 1988; Lindsey 1978; Videler 1993; Webb 1984a, 1984b, 1976; Weihs 1973, Weihs and Webb 1984). Morphological characteristics can be related to selective pressures by knowledge of the abilities of the fish and the functional significance of its morphological traits (Bock 1980). Differences in morphology that have a genetic basis can therefore be linked with the underlying processes of adaptive radiation by studies of the biomechanical significance of the divergent traits. In this study, knowledge of the distinctive morphological traits of the fishes, along with information on their swimming abilities can be used to link the morphologies of these fishes with the selective forces involved in their divergence. There are body shape differences that relate to differential selection for the methods of locating prey. Limnetics feed on zooplankton in the open water column (Larson 1972, 1976; Schiuter 1993; Schiuter and McPhail 1992) and must have good cruising ability to locate their prey. Selection on these fish has favoured traits that enhance steady swimming ability. Limnetics also exploit the complex habitat of the littoral zone during the breeding season (Larson 1976; Schiuter 1992) and are also adapted for good manoeuverability. Benthics live in the complex habitat throughout their lives (Larson 1976; Schiuter 1992). Selection on benthics has acted towards high manoeuverability but not good steady swimming ability. Selection due to differential resource use has probably lead to the divergence of body form of these fishes. Competition for resources has been shown to lead to character displacement (FjeldsA 1983; Grant and Grant 1989; Schiuter 1988; Schiuter and Grant 1984; Schiuter and McPhail 1992; Smith 1990; Werner 1977). Schiuter and McPhail (1992) presented evidence of character displacement among species of threespine sticklebacks from British Columbia and their results suggest that competition for food has played a critical role in the divergence  49  between species. Schiuter (1994) showed that habitat use efficiency by these sticklebacks is correlated with growth, indicating a relationship between morphology, habitat use, and fitness. My study supports the conclusion that differential resource use has lead to divergence in the morphological characteristics of these sticklebacks. The results of my study also suggest that selective pressure from predators has lead to consistent high escape fast-start performance. These fish use different methods to achieve the same goal of having a large body depth caudally to produce thrust for high performance of escape fast-starts. This similarity of performance suggests that the selection pressure from predators is, or has been very strong on both of these fishes. Recent investigations have shown a consistency among fishes to have high escape fast-start performance (Domenici and Blake 1991; Kasapi et al. 1993). Selection pressure from predation can therefore lead to convergence on morphologies that enhance thrust for high fast-start performance. In conclusion, this sympatric species pair of threespine stickleback has differential swimming performances that are a result of their morphological differences. Habitat use and morphological characteristics are linked by the influence that different traits have on swimming abilities. The morphological characteristics of these fishes have been under selective pressures from both resource competition and predation. Competition for resources has lead to character displacement and divergent selection while predation has lead to directional selection towards high escape fast-start performance. 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