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Fish fins and fast-starts: Multi-level analyses reveal functional variation within median fins of bluegill sunfish

Dissertation
Author: Brad A. Chadwell
Abstract:
Fins act as control surfaces by which fish can generate and react to hydrodynamic forces during a variety of locomotor behaviors. Within the ray-finned fish, the unique segmented, bilaminar design of their fin rays, for which they are named, provide the fish with the ability to independently control the degree of stiffness and curvature of each ray, enabling them to modulate the fin surface and the resultant hydrodynamic forces. While fin morphology and kinematic properties have been studied extensively, previous researchers have looked at the fins as a whole, overlooking variation between rays within the same fin. This work focused on describing the morphological and kinematic variation among fin-rays within the dorsal and anal fins of the bluegill sunfish, Lepomis macrochirus. Examining several musculoskeletal features of individual fin-rays within the dorsal and anal fins of bluegill, variation in (1) spine and ray lengths, (2) the proportion of the rays that were segmented or branched and (3) masses of the muscle slips that actuate the fin-rays were found; differences were correlated to longitudinal position within the fin. The quantitative results matched with a qualitative assessment of positional variations in fin-ray flexibility and joint mobility. Based on variation in morphological and biomechanical properties, regional differences in fin-ray kinematics during locomotion, allowing discrete regions of the fins to perform distinct functional roles, were proposed. Three-dimensional kinematics of selected individual fin-rays were quantified during the escape response of bluegill sunfish, a stereotypical behavior in which the fish undergoes a rapid acceleration and displacement to avoid predation. During this behavior, timing and magnitude of angular displacement and curvatures among fin-rays also differed predictably with longitudinal position. Most interestingly, a chordwise cupping of all three fins during Stage 1 of the fast-start was consistent with recent findings that median fins contribute to thrust forces generated by the body. Furthermore, a traveling wave along the lengths of the posterior rays of the soft dorsal and anal fins may be integral in determining the final direction of water jet to optimize the fin's thrust component, rather than generating only lateral, stabilizing forces.

IV TABLE OF CONTENTS Page LIST OF TABLES vi LIST OF FIGURES vii SYMBOLS AND ABBREVIATIONS x ABSTRACT xii INTRODUCTION TO THE DISSERTATION 1 CHAPTER 1 8 Musculoskeletal morphology and regionalization within the dorsal and anal fins of bluegill sunfish (Lepomis macrochirus) Abstract 9 Introduction 10 Methods and Materials 15 Results 22 Discussion 31 Literature Cited 43 CHAPTER 2 101 3-D kinematic analysis of the dorsal and anal fins during the fast-start of the bluegill sunfish {Lepomis macrochirus) I: Fin-ray orientation and movement Abstract 102 Introduction 103 Methods and Materials 107 Results 121 Discussion 127

V CHAPTER 3 181 3-D kinematic analysis of the dorsal and anal fins during the fast-start of the bluegill sunfish (Lepomis macrochirus) II: Fin-ray curvature Abstract 182 Introduction 183 Methods and Materials 186 Results 193 Discussion 196 Literature Cited 201 APPENDIX: Matlab codes for kinematic analysis and visualization 223 Introduction 224 Appendix A: Axial Codes 227 Appendix B: Fin Codes 234 Appendix C: Data Visualization 240 SCHOLASTIC VITA 246

LIST OF TABLES vi Page Table 2.1 Escape Response Kinematic Parameters by Fish 141 Table 2.2 Spiny Dorsal Fin-Ray Kinematic Parameters by Fish 142 Table 2.3 Kendall's W and Friedman's x2 for Spiny Dorsal Fin-Ray Kinematic Parameters 143 Table 2.4 Soft Dorsal Fin-Ray Kinematic Parameters by Fish 144 Table 2.5 Anal Fin-Ray Kinematic Parameters by Fish 145 Table 2.6 Kendall's W and Friedman's x2 for Soft Dorsal Fin-Ray Kinematic Parameters 146 Table 2.7 Kendall's Wand Friedman's x2 for Anal Fin-Ray Kinematic Parameters 147 Table 2.8 Multigroup fVfor Soft Dorsal vs. Anal Fin-Ray Kinematic Parameters 148 Table 3.1 Soft Dorsal Fin-Ray Curvature Parameters by Fish 203 Table 3.2 Anal Fin-Ray Curvature Parameters by Fish 204 Table 3.3 Kendall's W and Friedman's x2 for Soft Dorsal Fin-Ray Curvature Parameters 205 Table 3.4 Kendall's Wand Friedman's x2 for Anal Fin-Ray Curvature Parameters 206

vii LIST OF FIGURES Page Figure 1.1 Skeletal supports of the anal fin 45 Figure 1.2 Schematic of fin-ray joints and muscles 47 Figure 1.3 Illustration of bluegill sunfish and its fins 49 Figure 1.4 Length vs. spine position 51 Figure 1.5 Regional contributions to ray length vs. position 53 Figure 1.6 Regional lengths vs. ray position 55 Figure 1.7 Relative regional lengths vs. ray position 57 Figure 1.8 Rank order of regional lengths vs. ray position 59 Figure 1.9 Rank order of relative lengths vs. ray position 61 Figure 1.10 Difference in regional lengths vs. position between dorsal and anal rays 63 Figure 1.11 Difference in relative regional lengths vs. ray position 65 Figure 1.12 Rank order of regional differences vs. ray position 67 Figure 1.13 Rank order of relative regional differences vs. ray position 69 Figure 1.14 Contributions to fin-ray muscle mass vs. spine position 71 Figure 1.15 Fin-ray muscle mass vs. spine position 73 Figure 1.16 Relative fin-ray muscle mass vs. spine position 75 Figure 1.17 Rank order of fin-ray muscle mass vs. spine position 77 Figure 1.18 Rank order of relative fin-ray muscle mass vs. spine position 79 Figure 1.19 Contributions to fin-ray muscle mass vs. ray position 81 Figure 1.20 Fin-ray muscle mass vs. ray position 83

viii Figure 1.21 Relative fin-ray muscle mass vs. ray position 85 Figure 1.22 Rank order of fin-ray muscle mass vs. ray position 87 Figure 1.23 Rank order of relative fin-ray muscle mass vs. ray position 89 Figure 1.24 Difference in fin-ray muscle mass vs. position between dorsal and anal rays 91 Figure 1.25 Difference in relative fin-ray muscle mass vs. ray position 93 Figure 1.26 Rank order of muscle mass differences vs. ray position 95 Figure 1.27 Rank order of relative muscle mass differences vs. ray position .... 97 Figure 1.28 Muscle mass vs. fin-ray length 99 Figure 2.1 Stages of a C-start 149 Figure 2.2 The bluegill sunfish 151 Figure 2.3 Schematic of the flow tank set-up for video capture 153 Figure 2.4 The reconstructed dorsal fin surface and ray angles 155 Figure 2.5 Center of mass kinematics throughout a C-start 157 Figure 2.6 Axial turning rate throughout a C-start 159 Figure 2.7 Sweep angles of the spiny dorsal fin-rays 161 Figure 2.8 Sweep parameters of the spiny dorsal fin-rays 163 Figure 2.9 Span axis angles of the spiny dorsal fin-rays 165 Figure 2.10 Span axis parameters of the spiny dorsal fin-rays 167 Figure 2.11 Elevation and fin area parameters of the spiny dorsal fin-rays .... 169 Figure 2.12 Sweep angles of the soft dorsal and anal fin-rays 171 Figure 2.13 Sweep parameters of the soft dorsal and anal fin-rays 173 Figure 2.14 Span axis angles of the soft dorsal and anal fin-rays 175

ix Figure 2.15 Span axis parameters of the soft dorsal and anal fin-rays 177 Figure 2.16 Elevation and fin area parameters of the soft dorsal and anal fin-rays . 179 Figure 3.1 Curvature in the dorsal fin 207 Figure 3.2 Spanwise curvature of the soft dorsal fin-rays over time 209 Figure 3.3 Spanwise curvature of the anal fin-rays over time 211 Figure 3.4 Spanwise curvature parameters of the fin-rays 213 Figure 3.5 Chordwise curvature of the soft dorsal fin-rays over time 215 Figure 3.6 Chordwise curvature of the anal fin-rays over time 217 Figure 3.7 Chordwise curvature parameters of the fin-rays 219 Figure 3.8 Reconstructed bluegill and median fins 221

X SYMBOLS AND ABBREVIATIONS Chapter 1 AF Anal fin. ARy Rays of the anal fin. ASp Spines of the anal fin. Br Length of the branched portion of a ray, measured in mm. DF Dorsal fin, the spiny and soft dorsal fins collectively. DRy Rays of the dorsal fin. DSp Spines of the dorsal fin. mDepr Mass of the depressor muscle, measured in mg. mErec Mass of the erector muscle, measured in mg. mine Mass of the inclinator muscle, measured in mg. mTM Total mass of the inclinator, erector and depressor muscles, measured in mg. RL Total length of a ray, measured in mm. rBr Relative length of the branched portion of a ray, as a percent of total length. rDepr Relative mass of the depressor muscle, as a percent of total muscle mass. rErec Relative mass of the erector muscle, as a percent of total muscle mass, rlnc Relative mass of the inclinator muscle, as a percent of total muscle mass. rSg Relative length of the segmented portion of a ray, as a percent of total length. Sg Length of the segmented portion of a ray, measured in mm. SpL Total length of a spine, measured in mm sfD Soft dorsal fin. spD Spiny dorsal fin. UBr Length of the unbranched portion of a ray, measured in mm. USg Length of the unsegmented portion of a ray, measured in mm. AX Difference between anal and dorsal fin-rays, where X represents any length or mass parameter (absolute or relative). Chapters 2 and 3 Abbreviations COM Center of mass. sfA Soft region of the anal fin sfD Soft dorsal fin. spD Spiny dorsal fin. Rs Rostrum. Op Operculum. Ant Anterior trunk. Mid Middle trunk. Post Posterior trunk. DRy# Dorsal rays, where # indicates its numbered position within the fin. DSp# Dorsal spines, where # indicates its numbered position within the fin. ARy# Anal rays, where # indicates its numbered position within the fin. ASp# Anal spines, where # indicates its numbered position within the fin.

XI Subscripts Seg Body segment identifier. (0 Parameter values over the entire C-start sequence maxl First maximum peak event of a parameter. max2 Second maximum peak event of a parameter. tr Directional transition event, i.e., change in direction of rotation or orientation. r Fin-ray identifier Symbols A{r) Area between fin-rays. a Acceleration of the COM parallel to the fish trajectory. C Chord axis of the fin surface. cT Tangent to the chordwise curve. D Displacement of the center of mass. Fr Frontal axis, a.k.a., normal to the frontal plane. L Lateral axis, a.k.a. normal to the fin surface. 51 Stage 1 of the C-start. 52 Stage 2 of the C-start. S Span axis of the fin surface. Sg Sagittal axis, a.k.a., normal to the sagittal plane. sT Tangent to the spanwise curve. To Time zero. Tr Transverse axis, a.k.a., normal to the transverse plane. tX Time of a given parameter, where X is the event of a given parameter. v Velocity of the COM parallel to the fish trajectory. a Average span axis angle of a fin-ray. ArX Time difference between a given fin-ray parameter and its corresponding axial event, where X is the event of a given parameter. $ Average elevation of a fin-ray. Kspano Spanwise curvature, perpendicular to the fin surface. Kchord Chordwi se curvature, perpendicular to the fin surface and span axis. 8' Turning rate, i.e., the first time derivative of yaw. co Average sweep angle of a fin-ray.

xii ABSTRACT Brad A. Chadwell FISH FINS AND FAST STARTS: MULTI-LEVEL ANALYSES REVEAL FUNCTIONAL VARIATION WITHIN MEDIAN FINS OF BLUEGILL SUNFISH Dissertation under the direction of Miriam A. Ashley-Ross, Ph.D., Associate Professor of Biology Fins act as control surfaces by which fish can generate and react to hydrodynamic forces during a variety of locomotor behaviors. Within the ray-finned fish, the unique segmented, bilaminar design of their fin rays, for which they are named, provide the fish with the ability to independently control the degree of stiffness and curvature of each ray, enabling them to modulate the fin surface and the resultant hydrodynamic forces. While fin morphology and kinematic properties have been studied extensively, previous researchers have looked at the fins as a whole, overlooking variation between rays within the same fin. This work focused on describing the morphological and kinematic variation among fin-rays within the dorsal and anal fins of the bluegill sunfish, Lepomis macrochirus. Examining several musculoskeletal features of individual fin-rays within the dorsal and anal fins of bluegill, variation in (1) spine and ray lengths, (2) the proportion of the rays that were segmented or branched and (3) masses of the muscle slips that actuate the fin-rays were found; differences were correlated to longitudinal position within the fin. The quantitative results matched with a qualitative assessment of positional variations in fin-ray flexibility and joint mobility. Based on variation in morphological and biomechanical properties, regional differences in fin-ray kinematics

xiii during locomotion, allowing discrete regions of the fins to perform distinct functional roles, were proposed. Three-dimensional kinematics of selected individual fin-rays were quantified during the escape response of bluegill sunfish, a stereotypical behavior in which the fish undergoes a rapid acceleration and displacement to avoid predation. During this behavior, timing and magnitude of angular displacement and curvatures among fin-rays also differed predictably with longitudinal position. Most interestingly, a chordwise cupping of all three fins during Stage 1 of the fast-start was consistent with recent findings that median fins contribute to thrust forces generated by the body. Furthermore, a traveling wave along the lengths of the posterior rays of the soft dorsal and anal fins may be integral in determining the final direction of water jet to optimize the fin's thrust component, rather than generating only lateral, stabilizing forces.

1 INTRODUCTION TO THE DISSERTATION

2 'There is war between the larger and the lesser fishes: for the big fishes prey on the little ones' - Aristotle, The History of Animals, 350 BCE And the war continues to this day; though the little fishes are not without their defenses. Perhaps the most ubiquitous defense against predation among fish is the escape response, found in a wide range of fish phylogenies, including lamprey (Currie and Carlsen, 1987), sharks (Domenici et al., 2004), and within all branches of the Actinopterygii (Domenici and Blake, 1997; Eaton et al., 1977; Hale et al., 2002; Westneat et al., 1998). Similar escape responses have been described in amphibians as well (Azizi and Landberg, 2002; Hews and Blaustein, 1985). In most species studied, the Mauthner cell, a giant neuron, plays a primary role in the neural control of the escape response (reviewed by Eaton et al., 1977; Nissanov et al., 1990). The escape response is a stereotyped fast-start behavior, lasting < 1 s, in which the fish undergoes a burst of acceleration to distance itself from the threat. While there are variations in the form of the escape response, the C-start is the most common and has been studied extensively in a variety of teleost species (reviewed by Domenici and Blake, 1997). In the first mathematical model of the C-start, Weihs (1973) described three kinematic events: the preparatory stage (Stage 1), in which the body bends to one side, forming the aptly named 'C-shape'; the propulsive stroke (Stage 2), during which the fish accelerates away from the threat; and the variable stage (Stage 3), in which the fish either continues to swim away, glides to a stop or performs a braking maneuver. As a determining factor for avoiding predation, fish with greater escape response performances have a selective advantage (Ghalambor et al., 2003; Walker et al., 2005). It has been hypothesized that fish with enlarged dorsal and anal fins positioned close to the

3 caudal fin could act as an accessory tail to increase acceleration and thrust forces (Weihs, 1973), though it has been shown that this is not the only way to maximize performance as fish with different body forms achieve similar maximum accelerations (Webb, 1976). Despite the recognition that large median fins play an integral role in the performance of the escape response for fish that possess them, previous studies have paid little attention to the actual movement of the median fins. At most, it has been reported that the splaying of the fins (either some or all) occurs simultaneously with the onset of Stage 1 (Eaton et al., 1977) and/or that the fins are fully erected prior to, or soon after, the acceleration of Stage 2 (Webb, 1977; 1978). This alone provides no information as to what the fin is doing and how it might be contributing to the performance of the escape response. The large dorsal and anal fins of the bluegill sunfish (Lepomis macrochirus) have been shown to contribute to the thrust forces during steady swimming (Drucker and Lauder, 2001; Tytell, 2006) and most recently, the C-start (Tytell and Lauder, 2008). While hydrodynamic analyses are vital in demonstrating the contribution of the fins, they do not provide the details necessary to explain how the fins are interacting with the flow to generate and orient the flow of water. In order to provide further insight into the role of the median fins during the escape response, I carried out a multilevel analysis of the morphology and three-dimensional kinematics of individual fin-rays within the dorsal and anal fins of the bluegill sunfish. In Chapter 1,1 show that the morphology of the dorsal and anal fins of bluegill sunfish are not uniform, but instead individual fin-rays vary in their musculoskeletal design and biomechanical properties based on their position within the fins. I measured

4 the mass of the muscle slips for each fin-ray, and lengths of the individual spines and rays of the dorsal and anal fin, as well as the portion of each ray that was segmented vs. unsegmented and branched vs. unbranched. The pattern of variation in the musculoskeletal parameters among the fin-rays matched with the variation in the degree of flexibility and joint mobility observed, with the anterior supports of the fin being less flexible with a more restricted range of mobility than the posterior fin-rays. From the morphological regionalization of the fins, I propose distinct functional roles during locomotion, in which the stiffer anterior regions of the fins resist lateral forces and act to stabilize the fish, while the flexible posterior regions are used to direct the orientation of the flow to optimize the thrust component of the wake forces generated during locomotion. In Chapters 2 and 3,1 present detailed kinematic analyses of individual spines and rays of the dorsal and anal fins during the C-start escape response of the bluegill sunfish. True three-dimensional coordinates of the body and fin-rays were digitized from video sequences captured by three synchronized high-speed cameras. In Chapter 2,1 quantify movement and orientation of the fin-rays, relative to the body axis. As predicted from the morphological results, maximum angular displacement was greatest among the more flexible and mobile posterior rays of the fin. Second, the timing of angular displacement supported the hypothesis that the fins are actively resisting hydrodynamic forces that would tend to oppose the movement of the fins. In Chapter 3,1 extend the kinematic analysis of the soft dorsal and anal fins by examining the spanwise and chordwise curvature of the fin surface throughout the C-start sequence. Unlike the maximum angular displacements, maximum curvature among the

5 fin-rays did not vary consistently with position, though the spanwise curvature of the posterior fin-rays tended to be greater than the anterior fin-rays. Timing of maximum curvature was either uniform among the fin-rays or showed no consistent pattern with fin-ray position. However, the fin surface underwent a stereotypical postero-distal undulation. Among the anterior fin-rays, a wave of chordwise curvature in the fin surface traveled posteriorly along the chord length of the fin over time. Within the posterior region of the fin, a wave of spanwise curvature traveled distally along the lengths of the fin-rays, increasing in magnitude. Initiation of the surface undulation started midway though Stage 1 of the C-start, reaching the trailing edge of the fins soon after the start of Stage 2. Supporting the previous electromyographic (EMG) studies of the inclinator muscles of the dorsal fin (Jayne et al., 1996) and hydrodynamic (Tytell and Lauder, 2008) studies of the median fins during the C-start of the bluegill sunfish, I have shown that the kinematic patterns of the individual fin-rays within the median fins vary to produce a complex, yet stereotyped undulation of the fin surface. From the regional variations observed, I suggest functionally distinct roles within the fins. Specifically, the elevation and cupping of the anterior spiny dorsal fin increases the lateral depth of the body, thereby increasing the volume of water upon which the fish can exert force to generate acceleration. Second, a chordwise undulation within the anterior region of the soft dorsal and anal fins moves the water posteriorly along the fin, helping to overcome the inertia of the water. Third, a spanwise undulation of the posterior fin region accelerates the flow of the water caudally to optimize the thrust component of the hydrodynamic forces generated by the fin. The simple outward appearance of the median

6 fins belies the complexity of their design and function. To truly understand the intricacy of the fins as control surface requires the integration of detailed analysis at all levels of study: morphology, biomechanical properties, EMG, kinematics and hydrodynamics. All three chapters are in preparation to be submitted for publication. Chapter 1 will be submitted to the Journal of Morphology with Ben Hunter and Miriam A. Ashley- Ross as co-authors. Chapters 2 and 3 will be submitted to the Journal of Experimental Biology, with Emily M. Standen, George V. Lauder and Miriam A. Ashley-Ross as co authors. LITERATURE CITED Azizi E, Landberg T. 2002. Effects of metamorphosis on the aquatic escape response of the two-lined salamander (Eurycea bislineata). J Exp Biol 205:841-849. Currie SN, Carlsen RC. 1987. Functional significance and neural basis of larval lamprey startle behaviour. J Exp Biol 133:121-135. Domenici P, Blake RW. 1997. The kinematics and performance offish fast-start swimming. J Exp Biol 200:1165-1178. Domenici P, Standen EM, Levine RP. 2004. Escape manoeuvres in the spiny dogfish {Squalus acanthias). J Exp Biol 207:2339-2349. Drucker EG, Lauder GV. 2001. Locomotor function of the dorsal fin in teleost fishes: Experimental analysis of wake forces in sunfish. J Exp Biol 204:2943-2958. Eaton RC, Bombardieri RA, Meyer DL. 1977. The Mauthner-initiated startle response in teleost fish. J Exp Biol 66:65-81. Ghalambor CK, Walker JA, Reznick DN. 2003. Multi-trait selection, adaptation, and constraints on the evolution of burst swimming performance. Integr Comp Biol 43:431-438. Hale ME, Long JH, Jr., McHenry MJ, Westneat MW. 2002. Evolution of behavior and neural control of the fast-start escape response. Evolution 56:993-1007. Hews DK, Blaustein AR. 1985. An investigation of the alarm response in Bufo boreas and Rana cascadae tadpoles. Behavioral and Neural Biology 43:47-57.

7 Jayne BC, Lozada GF, Lauder GV. 1996. Function of the dorsal fin in bluegill sunfish: Motor patterns during four distinct locomotor behaviors. J Morphol 228:307-326. Nissanov J, Eaton RC, DiDomenico R. 1990. The motor output of the Mauthner cell, a reticulospinal command neuron. Brain Res 517:88-98. Tytell ED. 2006. Median fin function in bluegill sunfish Lepomis macrochirus: Streamwise vortex structure during steady swimming. J Exp Biol 209:1516-1534. Tytell ED, Lauder GV. 2008. Hydrodynamics of the escape response in bluegill sunfish, Lepomis macrochirus. J Exp Biol 211:3359-3369. Walker JA, Ghalambor CK, Griset OL, McKenney D, Reznick DN. 2005. Do faster starts increase the probability of evading predators? Funct Ecol 19:808-815. Webb PW. 1976. The effect of size on the fast-start performance of rainbow trout Salmo gairdneri, and a consideration of piscivorous predator-prey interactions. J Exp Biol 65:157-177. Webb PW. 1977. Effects of median-fin amputation on fast-start performance of rainbow trout (Salmo gairdneri). J Exp Biol 68:123-135. Webb PW. 1978. Fast-start performance and body form in seven species of teleost fish. J Exp Biol 74:211-226. Weihs D. 1973. The mechanism of rapid starting of slender fish. Biorheology 10:343- 350. Westneat MW, Hale ME, McHenry MJ, Long JH. 1998. Mechanics of the fast-start: Muscle function and the role of intramuscular pressure in the escape behavior of Amia calva and Polypteruspalmas. J Exp Biol 201 (Pt 22):3041-3055.

8 CHAPTER 1 MUSCULOSKELETAL MORPHOLOGY AND REGIONALIZATION WITHIN THE DORSAL AND ANAL FINS OF BLUEGILL SUNFISH (LEPOMISMACROCHIRUS)

9 ABSTRACT Ray-finned fishes actively control the shape and orientation of their fins to either generate or resist hydrodynamic forces. Due to the emergent mechanical properties of their segmented, bilaminar fin rays, lepidotrichia, and actuation by multiple muscles, fish can control the rigidity and curvature of individual rays independently, thereby varying the resultant forces across the fin surfaces. Expecting that differences in fin-ray morphology should reflect variation in their mechanical properties, we measured several musculoskeletal features of individual spines and rays of the dorsal and anal fins of bluegill sunfish, Lepomis macrochirus, and assessed their mobility and flexibility. We separated the fin-rays into four groups based on the fin (dorsal or anal) or fin-ray type (spine or ray) and measured the length of the spines/rays and the mass of the three median fin-ray muscles: the inclinators, erectors and depressors. Within the two ray groups, we measured the portion of the rays that were segmented vs. unsegmented and branched vs. unbranched. For the majority of variables tested, we found that variations between fin-rays within each group were significantly related to position within the fin and these patterns were conserved between the dorsal and anal rays. Based on positional variations in fin-ray and muscle parameters, we suggest that each fin can be divided into anterior and posterior regions that perform different functions when interacting with the surrounding fluid. Specifically, we suggest that the stiffer anterior rays of the soft dorsal and anal fins maintain stability and keep the flow across the fins steady. The posterior rays, which are more flexible with a greater range of motion, fine-tune their stiffness and orientation, directing the resultant flow in a direction to generate lateral and thrust forces, thus acting as accessory caudal fins.

10 INTRODUCTION Actinopterygian fishes can actively control the shape and curvature of their fins due to the unique design feature of the supporting bony fin-rays (Fig. 1.1). Named for this defining characteristic, ray-finned fishes are able to adjust the stiffness and curvature of individual fin-rays, known as lepidotrichia, allowing for fine-tuned manipulation of the fin surface and resulting fin conformation (Alben et al., 2007; 1971; Lauder, 2006; McCutchen, 1970; Videler, 1977). Although detailed structural descriptions of lepidotrichia and their mechanical properties are available from only a few teleost species: gourami and goldfish (Haas, 1962); trout (McCutchen, 1970); tilapia (Geerlink and Videler, 1987; Videler, 1977) and bluegill sunfish (Alben et al., 2007), the general structure of lepidotrichia has been found to be consistent across all ray-finned fishes examined (Arita, 1971; Eaton, 1945; Goodrich, 1904). Each lepidotrich is composed of two halves, or hemitrichia (Fig. 1.1C), located opposite each other on each side of the fin bound together by flexible collagen fibers (Haas, 1962; Videler, 1977). The proximal third of each hemitrich is a single piece of unsegmented bone, while the remaining portion, which is often branched, consists of several bony segments (Fig. 1.1). The proximal end of each unsegmented bone expands to form the head, which articulates with the underlying endoskeletal fin supports and serves as the attachment sites for the muscles of the fin-ray (Figs. 1.1 and 1.2). The most distal segments are bound by an unmineralized, extracellular matrix of collagenous fibrils, known as actinotrichia (Haas, 1962; Videler, 1977), which prevent the distal segments from being able to move relative to one another.

11 In the dorsal and anal fins, three muscles attach to the heads of both hemitrichia: the inclinator, erector and depressor muscles (Winterbottom, 1974). Originating from the fascia between the skin and axial musculature, the inclinator inserts laterally onto the head and is responsible for lateral movement of the fin-ray (Fig. 1.2B). The erector and depressor muscles originate from the lateral surfaces of the rays' endoskeletal support (the pterygiophores) and insert onto anterolateral and posterolateral processes of the head (erector and depressor, respectively) and serve to erect or depress the fin-ray (Fig. 1.2B). The complex arrangement described above, coupled with the mechanical properties of the composite materials comprising the structure, allows the fish to control the bending and stiffness of individual lepidotrichia. A force parallel to the long axis of the lepidotrich applied to one side displaces the two hemitrichia relative to one another, causing the ray to curve to one side and stiffen. Previously thought to be a passive reaction to hydrodynamic loading during swimming to prevent over bending and to maximize propulsive thrust generated by the fins (McCutchen, 1970), later studies demonstrated that fish have a more active role in controlling the ray curvature and stiffness (Alben et al., 2007; Arita, 1971; Geerlink and Videler, 1987; Videler, 1977). Fish can activate fin muscles of the rays to not only reduce or prevent fin bending but to potentially modulate the hydrodynamic forces generated by actively controlling the shape and rigidity of the entire fin surface (Alben et al., 2007). In derived teleost fishes, primarily within Acanthopterygii, specialized lepidotrichia composed of a single unbranched bony element, known as spines, support the anterior regions of the dorsal and anal fins (Fig. 1.1 A and 1.3). Spines typically have the same complement of muscles attaching to them as lepidotrichia (Fig. 1.2D); however,

12 spine movement is restricted primarily to elevation/depression, with little to no lateral deflection (Eaton, 1945; Geerlink and Videler, 1973). Widely accepted as an anti- predator device (Hoogland et al., 1956), the suggested role of the spines during locomotion is to act as a keel or cutwater (Eaton, 1945). However, to our knowledge, no study has investigated what hydrodynamic role, if any, spiny regions of the median fins play during swimming behaviors, with the exception of the observation that the orientation and velocity of flow at the region of the spiny dorsal fin does not change during slow swimming speeds (Drucker and Lauder, 2001a). Within the literature, the wide range of locomotor behaviors observed among ray- finned fishes has long been attributed to the variability in the anatomy and mechanics of the fins used for a particular swimming mode, e.g. undulation of the body and caudal fin vs. movement of the pectoral fins (see Blake, 2004; Lauder, 2006; Walker, 2004 for recent reviews). Despite the observation that fish are capable of controlling fin conformation depending on the swimming behavior employed, few studies have examined whether variations in fin-ray morphology within the fins exist and what effect they may have on their mechanical properties and/or kinematic parameters during locomotion (Arita, 1971; Lauder and Madden, 2007; Standen and Lauder, 2005; Taft et al., 2008). The focus of studies for more than a decade, the bluegill sunfish, Lepomis macrochirus (Perciformes), displays a repertoire of different locomotor behaviors. The combination of fins used and their kinematic patterns are equally varied, based on the swimming mode employed (Drucker and Lauder, 2000; 2001a; b; Jayne et al., 1996; Lauder and Drucker, 2004; Lauder and Madden, 2007; Standen and Lauder, 2005). For

Full document contains 262 pages
Abstract: Fins act as control surfaces by which fish can generate and react to hydrodynamic forces during a variety of locomotor behaviors. Within the ray-finned fish, the unique segmented, bilaminar design of their fin rays, for which they are named, provide the fish with the ability to independently control the degree of stiffness and curvature of each ray, enabling them to modulate the fin surface and the resultant hydrodynamic forces. While fin morphology and kinematic properties have been studied extensively, previous researchers have looked at the fins as a whole, overlooking variation between rays within the same fin. This work focused on describing the morphological and kinematic variation among fin-rays within the dorsal and anal fins of the bluegill sunfish, Lepomis macrochirus. Examining several musculoskeletal features of individual fin-rays within the dorsal and anal fins of bluegill, variation in (1) spine and ray lengths, (2) the proportion of the rays that were segmented or branched and (3) masses of the muscle slips that actuate the fin-rays were found; differences were correlated to longitudinal position within the fin. The quantitative results matched with a qualitative assessment of positional variations in fin-ray flexibility and joint mobility. Based on variation in morphological and biomechanical properties, regional differences in fin-ray kinematics during locomotion, allowing discrete regions of the fins to perform distinct functional roles, were proposed. Three-dimensional kinematics of selected individual fin-rays were quantified during the escape response of bluegill sunfish, a stereotypical behavior in which the fish undergoes a rapid acceleration and displacement to avoid predation. During this behavior, timing and magnitude of angular displacement and curvatures among fin-rays also differed predictably with longitudinal position. Most interestingly, a chordwise cupping of all three fins during Stage 1 of the fast-start was consistent with recent findings that median fins contribute to thrust forces generated by the body. Furthermore, a traveling wave along the lengths of the posterior rays of the soft dorsal and anal fins may be integral in determining the final direction of water jet to optimize the fin's thrust component, rather than generating only lateral, stabilizing forces.