Functional regionalization of the pectoral fin of the benthic longhorn sculpin during station holding and swimming

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1 Journal of Zoology Functional regionalization of the pectoral fin of the benthic longhorn sculpin during station holding and swimming N. K. Taft 1, G. V. Lauder 2 & P. G. A. Madden 2 1 Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts Amherst, Amherst, MA, USA 2 Museum of Comparative Zoology, Harvard University, Cambridge, MA, USA Journal of Zoology. Print ISSN Keywords fish; sculpin; benthic; swimming; locomotion; three-dimensional kinematics; pectoral fin. Correspondence Natalia K. Taft, Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts Amherst, 211 Morrill Science Center South, 611 North Pleasant St, Amherst, MA 01003, USA. natashak@bio.umass.edu Editor: Jean-Nicolas Volff Received 11 February 2008; revised 1 May 2008; accepted 9 May 2008 doi: /j x Abstract Studies of the kinematics of the pectoral fins in fishes have focused on fins as devices for propulsion or maneuvering. Studying pectoral fin function in benthic fishes is an opportunity to understand how the fins are used in a broader range of fin-based behaviors, especially those involving substrate contact. Morphological specializations of the pectoral fins, hypothesized adaptations for substrate contact, have been described for several benthic fish groups. These specializations include, but are not limited to, reduced webbing between ventral rays as well as thickening and shortening of these rays compared with the dorsal rays. Our focal species, the benthic longhorn sculpin, Myoxocephalus octodecimspinosus, possesses these morphological specializations, which divide the fin loosely into dorsal and ventral regions. Our goal was to investigate the functional consequences of these specializations, if any. First, we used high-speed video to examine the motion of the pectoral fins during swimming and station holding on the bottom, the first such study for a benthic fish. We found that longhorn sculpin do not oscillate their pectoral fins during swimming. Rather, the pectoral fins are held in a steady laterally extended posture. Oscillations of the body, median fins and caudal fin are used for propulsion. The shape of the fin also changes dramatically as the fish moves from station holding to swimming. Second, we measured the curvature of the individual fin rays that support and control the shape and movement of the pectoral fins. We did this to examine whether morphological specialization of the fin rays influences fin ray curvature. Individual fin rays in different fin regions show consistently different patterns of bending regardless of behavior. We propose that the pectoral fin is divided into functional as well as morphological regions. The fin rays in each functional region have distinct roles during swimming and substrate contact. Introduction The transition from a pelagic to a benthic lifestyle has occurred in several groups of fishes (Aleev, 1969; Gosline, 1994). This shift has been accompanied by morphological changes in the structure of the pectoral fins (Gosline, 1994). The pectoral fins of most fishes are used for propulsion, maneuverability and/or stability in the water column (Walker & Westneat, 2002; Drucker & Lauder, 2003; Drucker, Walker & Westneat, 2006). However, the pectoral fins of benthic fishes are often used for behaviors involving substrate contact. For example, pectoral fins aid in digging, burrowing, probing, clinging, crawling, supporting the body of the fish at rest or actively resisting displacement in flow during station holding (Lundberg & Marsh, 1976; Webb, 1989; Brandstatter et al., 1990; Gosline, 1994; Jamon et al., 2007). It has been hypothesized that the pectoral fins of benthic fishes evolved from an ancestral pelagic condition (Gosline, 1994). Specifically, it has been suggested that the benthic pectoral fin evolved from a condition of a relatively uniform morphology into a benthic morphology characterized by distinct dorsal and ventral morphological regions, the ventral region specialized for substrate contact (Wagner, 1989). In this study, we explore the morphological and functional specializations of the pectoral fins in the scorpaeniform fish Myoxocephalus octodecimspinosus, the longhorn sculpin. Our goal is to better understand regionalization of the pectoral fins in benthic fishes. Scorpaeniform fishes are a group noted for diversity of morphological adaptations, including regionalization, of the pectoral fins associated with a benthic lifestyle (Gosline, 1994). The evolution of regionalization may provide a way to decouple the conflicting functional demands of swimming and substrate contact on the pectoral fins (Brandstatter et al., 1990). However, functional differences in the morphologically distinct regions of the pectoral fins in benthic fishes have not been examined previously. Journal of Zoology ]] (2008) 1 9 c 2008 The Authors. Journal compilation c 2008 The Zoological Society of London 1

2 Functional regionalization of the pectoral fin N. K. Taft, G. V. Lauder and P. G. A. Madden To examine functional differences within the pectoral fin, we focus on the curvature and position of the individual pectoral fin rays, or lepidotrichia, that support the pectoral fins during station holding and swimming. The curvature and relative movement of individual fin rays determines the shape and function of the pectoral fin in most fishes (Geerlink, 1987, Geerlink & Videler 1987; Standen & Lauder, 2005; Lauder et al., 2006: Alben, Madden & Lauder, 2007). Studying specializations of the pectoral fins of benthic fishes will allow us to better understand the evolutionary mechanisms underlying patterns of morphological change associated with specialization for benthic habitats. We use three-dimensional kinematics and measurements of individual fin ray curvature in the longhorn sculpin to address three specific questions. First, how are the pectoral fins of this primarily benthic species used during swimming in the water column versus during benthic station holding? Second, do the fin rays in the dorsal and ventral regions of the pectoral fin show distinct patterns of curvature? Third, does the curvature of individual fin rays vary between station holding and swimming behaviors? We predict that there are inherent differences in curvature associated with the morphological regionalization of the pectoral fin within and among individual fin rays during station holding versus swimming. Materials and methods Fish We collected data from four individual longhorn sculpins M. octodecimspinosus (Mitchill, 1814). Fish were maintained in the laboratory in 1.5-m-diameter holding tanks in saltwater (30 ppt) under a 12:12 h L:D photoperiod with a mean water temperature of 10 1C (plus or minus 2 1C). The four individuals in this study ranged in total length from 26 to 28 cm. Behavioral observations We placed individual longhorn sculpin in a variable-speed flow tank with a central working area 28 cm wide, 28 cm deep and 80 cm long as in our previous research on fish pectoral fin function (Wilga & Lauder, 1999; Drucker & Lauder, 2003, 2005; Standen & Lauder, 2005). We elicited steady horizontal swimming and filmed fish using two synchronized high-speed video cameras [Photron Fastcam pixels (ventral) and a Photron APX system pixels (lateral) (Photron, San Francisco, CA)] operating at 125 frames s 1, to characterize the relative position and curvature of the individual fin rays. We filmed four individual fish during station holding and during steady swimming. We began filming each fish when the pectoral fins were in contact with the substrate and ended when the fin was maximally extended and held in place during slow swimming. During station holding the ventral portion of the pectoral fins was in contact with the floor of the flow tank. During swimming no part of the pectoral fins was in contact with the substrate. The flow tank was set at 1 body length s 1 or less, but actual fish swimming speeds varied greatly as fish accelerated off the bottom. We filmed and digitized the left pectoral fins of each individual. The station holding bouts are highly stereotyped; therefore, we focused our efforts on collecting video of the pectoral fin during swimming. Each swimming sequence contained a minimum of three consecutive tail beats. For the analysis, one frame was selected and digitized for each station holding bout. One frame depicting the fin when it was maximally extended and the fish was swimming steadily was selected and digitized for each of three to six swimming bouts. Morphology After videos for kinematic analysis were taken, fish were sacrificed. The external morphology of the pectoral fins was examined in each individual to describe morphological differences of fin rays in the dorsal and ventral regions of the pectoral fin. In addition, one X-ray photograph of the pectoral fin of an additional individual was taken to visualize the skeletal elements of the pectoral girdle and fin rays. Three-dimensional analysis of fin ray curvature We calibrated the cameras using the system developed by Standen & Lauder (2005). We filmed images of a calibration cube in both lateral and ventral views. The cube had no less than 23 points visible in both camera views. We then used a direct linear transformation method to calculate the positions of the cameras relative to each other and to the calibration cube. With this method, we were able to accurately calculate the three-dimensional coordinates of any point on the pectoral fin. Using a custom Matlab program, we calibrated the cameras and digitized the images. Every other fin ray was digitized proximo-distally at 20% intervals, beginning with the most ventral ray 18. The most dorsal ray, ray 1, was also digitized because it makes up the leading edge of the fin during swimming; 10 rays were digitized in all for each fish. These points provided the three-dimensional coordinates of fin ray position at 0% (most proximal), 20, 40, 60, 80 and 100% (most distal) of the total length of each individual fin ray. We digitized the individual fin rays during station holding and steady swimming. The coordinates were imported into Matlab, where we fit a three-dimensional parametric cubic spline through the three-dimensional coordinates of the six equally spaced points along each pectoral fin ray. We calculated curvature along the spline for each ray using the following equation: k ¼jdT=dsj where T is the unit tangent vector and s is the arc length of the curve. Curvature (k) is defined as the change in the unit tangent vector divided by the change in the arc length curve (Stewart, 2003). We sampled curvature from the fitted 2 Journal of Zoology ]] (2008) 1 9 c 2008 The Authors. Journal compilation c 2008 The Zoological Society of London

3 N. K. Taft, G. V. Lauder and P. G. A. Madden Functional regionalization of the pectoral fin splines at intervals of 10% distance along the total length of the fin ray (0% being most proximal, 100% most distal) to allow us to compare patterns of curvature between rays for each behavior as well as within a single ray between behaviors. Fin ray curvature as defined in this paper measures the true three-dimensional curvature of the fin rays. sc 1 Dorsal m 8 Statistics We used a repeated measures ANOVA to model the effect of fin ray number, behavior (station holding or swimming) and their interaction on the curvature between fin rays and along the proximo-distal length of each fin ray. We compared the location of maximum curvature, total curvature and shape of the fin ray along its proximal distal length among fin rays. The total curvature is the integral of instantaneous curvature taken over the whole length of the fin ray. The shape of the ray refers to a function relating each point along the proximo-distal length of a fin ray to the instantaneous curvature of the fin ray at that point. Shape was analyzed both within each ray and among fin rays. We also used post hoc least square mean contrasts to examine differences between individual fin rays that we detected in our model. In addition, we modeled the effect of fin ray and location along fin ray on curvature for each behavior separately to see whether patterns of curvature of each fin ray differed between behaviors. We performed the same post hoc least square mean contrasts for each behavior separately as we did for the analysis with behaviors pooled together. All statistical analyses were conducted using the program JMP v. 5.0 (JMP, 2002). Results Morphology Pectoral fin ray number in this species ranges from 17 to 18 (Collette & Klein-MacPhee, 2002). Individuals in our kinematic analysis all had 18 pectoral fin rays. An X-ray of the pectoral fin shown in Fig. 1 shows the skeletal anatomy of the pectoral girdle and individual fin rays in more detail. This individual had 17 pectoral fin rays. There are morphological differences among dorsal versus ventral fin rays. Ventral rays 10 17/18 are shorter, have a reduction in fin membrane between adjacent rays, are thicker and have a fleshy appearance that resembles specializations of the ventral hook field described previously for blennies (Brandstatter et al., 1990). The remaining eight dorsal fin rays are longer and thinner than the ventral rays and the membrane between adjacent rays extends to the distal tip of each dorsal fin ray. The morphological boundary between fin rays, most clearly defined by ventral membrane reduction, lies between fin rays 9 and 10. All fin rays in M. octodecimspinosus are unbranched distally. cl co Kinematics ac 17 Ventral =10 mm Figure 1 X-ray of the pectoral girdle of longhorn sculpin, Myoxocephalus octodecimspinosus, from an individual with 17 fin rays. Fin rays 1, 8 and 17 are labeled and indicated by white lines. Abbreviations for these structures are as follows: ac, actinost; cl, cleithrum; co, coracoid; fr, fin rays (lepidoptrichia); m, fin membrane; sc, scapula. Pectoral fin posture differs consistently between station holding and swimming. During station holding, the ventral fin rays are positioned anterior to the dorsal fin rays and the dorsal rays are adducted into contact with the body, although not necessarily with each other. In contrast, during swimming the ventral fin rays are adducted into contact with the body while the dorsal rays are drawn anteriorly and folded over the ventral rays laterally. The fin is held in a steady, extended conformation for the duration of a swimming bout. The difference in pectoral fin conformation between station holding and swimming for longhorn sculpin can be seen in Fig. 2. The change in position of dorsal and ventral fin rays as sculpin transition from benthic station holding to swimming can be seen most clearly in the ventral view (Fig. 2c and d). The posterior position of the dorsal rays (white arrow) relative to the ventral rays (black arrow) during substrate contact is clearly visible in Fig. 2c. The adduction of the ventral rays (black arrow) and drawing anterior of the dorsal rays is clearly visible (Fig. 2d). In order to achieve this swimming posture, the dorsal portion of the fin is folded laterally and anteriorly over the adducted ventral rays. We have divided the transition of pectoral fin posture from station holding to swimming into four stages for ease of description and visualization. These stages are (1) station holding, (2) expansion/adduction, (3) flip and (4) steady swimming (Fig. 3a h). During station holding, the ventral fin rays of the pectoral fin are in contact with the substrate and anterior to the dorsal region of the pectoral fin (Fig. 3a and e). The dorsal, posterior region of the fin is adducted fr Journal of Zoology ]] (2008) 1 9 c 2008 The Authors. Journal compilation c 2008 The Zoological Society of London 3

4 Functional regionalization of the pectoral fin N. K. Taft, G. V. Lauder and P. G. A. Madden (a) (c) (b) (d) Figure 2 Posture of the left pectoral fin of the longhorn sculpin during (a, c) station holding and (b, d) swimming. Station holding and swimming postures are compared in (a, b) lateral and (c, d) ventral views. White arrows indicate the position of the most dorsal fin ray. Black arrows indicate the position of the most ventral fin ray. Color balance of photos has been adjusted for clarity. The grid behind the fish in lateral view is 2 cm 2cmsquare. (a) (e) (b) (f) (c) (g) (d) (h) Figure 3 Illustration of the kinematics of the left pectoral fin of a longhorn sculpin transitioning from station holding to swimming. Adjacent images are simultaneous lateral (left) and ventral (right) views at each of four stages during the transition. All images are taken from a single video sequence (125 frames/second). The four stages in the transition from station holding to swimming are (a, e) station holding, (b, f) fin expansion, (c, g) fin flip and (d, h) swimming. Red arrows indicate the motion of dorsal fin rays. Blue arrows represent the motion of the ventral fin rays. 4 Journal of Zoology ]] (2008) 1 9 c 2008 The Authors. Journal compilation c 2008 The Zoological Society of London

5 N. K. Taft, G. V. Lauder and P. G. A. Madden Functional regionalization of the pectoral fin into contact with the lateral surface of the fish. Next, during the expansion phase (Fig. 3b and f) the individual fin rays are rapidly fanned apart. This increase in surface area occurs just before the fin is rapidly adducted. In some cases, the fin is expanded and adducted or flapped several times before the fish successfully lifts itself from the substrate. Then, during the flip phase after the fin has been adducted, the two most dorsal rays are drawn laterally and anteriorly over the adducted ventral rays (Fig. 3c and g). These rays make up the new leading edge of the fin in preparation for swimming. Finally, in the steady swimming stage all of the dorsal rays are drawn cranio-laterally into the extended posture (Fig. 3d and h). The eight dorsal rays that are used to support the folded fin follow the two most dorsal rays (1 and 2) that make up the leading edge. The 10 most ventral rays remain adducted and come into contact with the body. After folding, the fin surface that had been lateral during station holding became ventral and the formerly medial surface became directed dorsally. In this way the dorsal region of the fin is folded over on top of the ventral region to form a steady extended horizontal surface during steady swimming. The pectoral fin remains in folded conformation during swimming until the fish returns to the substrate. At that point the dorsal portion of the fin is rapidly adducted as the ventral rays are extended laterally and anteriorly. Curvature among and within individual fin rays The curvature of all fin rays was higher at all locations along the proximo-distal length of each fin ray during substrate contact than during swimming (see Fig. 4, F 1,156 = o0.0001). In addition, the shape of the curve along the proximo-distal length of the fin rays varied significantly with behavior (Pillai s Trace 10,147 =o0.0001) (see Fig. 5). During substrate contact, the curvature was higher at the 0.15 Station holding Swimming Curvature (1/mm) Curvature (1/mm) ii i iv iii Proximal 0.5 Swimming Distance along fin ray (%) Proximal Station holding Distance along fin ray (%) i ii iv iii Distal i ii iii iv Distal Figure 5 Illustration of the total curvature along the proximo-distal length of the pectoral fin rays. Fin rays are grouped by post-hoc contrast analysis (see text for discussion of statistical analysis, and Table 1 for F-statistics). Group 1 (solid black line) is composed of ray 18, the most ventral ray. Group 2 (solid grey line) is composed of ray 16, the second most ventral ray. Group 3 (dotted black line) consists of rays 4 14, the middle rays. Group 4 (dotted grey line) is composed of rays 1 and 2, the two most dorsal rays. Vertical bars show standard error at each 10% interval along the proximo-distal length of the rays. Curvature (1/mm) Proximal Distance along fin ray (%) Distal Figure 4 Mean curvature of all fin rays during station holding (black line) versus swimming (grey line) along the proximo-distal length of the rays with standard error (vertical bars). proximal and distal ends of the rays for both behaviors (see Fig. 4). The average magnitude of the curvature among individual fin rays varied significantly regardless of behavior (F 9,156 =o0.0001). Our post hoc analyses of curvature allowed us to examine patterns of curvature both among and within the fin rays in more detail. We performed our contrasts for each behavior separately. Our set of contrasts first compared the average magnitude of the curvature and then, separately, the shape of the dorsal rays 1, 2, 4, 6 and 8 to that of the ventral rays, 10, 12, 14, 16 and 18 (see Table 1). The dorsal and ventral regions differed significantly in the average magnitude of curvature during station holding and swimming. However, further examination of our model suggested that these differences between these regions of the pectoral fin are driven largely by the magnitude and shape of the curvature of Journal of Zoology ]] (2008) 1 9 c 2008 The Authors. Journal compilation c 2008 The Zoological Society of London 5

6 Functional regionalization of the pectoral fin N. K. Taft, G. V. Lauder and P. G. A. Madden Table 1 Post hoc least square mean contrast analyses of total curvature and shape of curvature along the proximo-distal length among pectoral fin rays of Myoxocephalus octodecimspinosus, the longhorn sculpin Exact F Prob4F Magnitude of curvature (d.f. numerator=1, d.f. denominator=156) Dorsal (1 8) versus ventral o (10 18) (hold) Dorsal (1 8) versus ventral o (10 18) (swim) Group 1 versus 2, 3 and 4 (hold) o Group 1 versus 2, 3 and 4 (swim) o Group 2 versus 3 and 4 (hold) o Group 2 versus 3 and 4 (swim) o Group 3 versus 4 (hold) 6.03 o Group 3 versus 4 (swim) o Shape along proximo-distal length of ray (d.f. numerator=10, d.f. denominator=147) Dorsal (1 8) versusventral 4.86 o (10 18) (hold) Dorsal (1 8) versus ventral 8.44 o (10 18) (swim) Group 1 versus 2, 3 and 4 (hold) o Group 1 versus 2, 3 and 4 (swim) o Group 2 versus 3 and 4 (hold) 7.53 o Group 2 versus 3 and 4 (swim) 5.45 o Group 3 versus 4 (hold) 3.99 o Group 3 versus 4 (swim) 5.58 o the fin rays at the dorsal and ventral edges of the pectoral fin, particularly during station holding. We broke the fin up into four groups based on the total curvature and shape of the fin rays for both behaviors in our model (Fig. 5). Group 1 consists of the most ventral fin ray, 18. Group 2 is made up of ray 16, the second most ventral ray. Group 3 is made up of rays 4 14, the middle of the fin. Group 4 is made up of the dorsal fin rays, 1 and 2, that make up the leading edge during swimming. Figure 5 shows the curvature of the fin rays in each group along the proximodistal length of the fins rays. We performed post hoc least square mean contrasts for each of these groups to determine whether there are significant differences in total curvature and shape among these post hoc groupings. Table 1 gives the F-statistics for these contrasts. Our first set of contrasts examined differences in the average magnitude of curvature for each group. The magnitude of curvature for group 1 was significantly higher than the curvature for all other groups during station holding and swimming. Group 2 was significantly different from groups 3 and 4 during both station holding and swimming. Finally, groups 3 and 4 had significantly different average curvature magnitudes during station holding, but not during swimming (see Table 1, Fig. 5). Our second set of contrasts between groups examined differences in shape along the rays among the groups. Group 1 differs significantly in shape from groups 2, 3 and 4 for both behaviors. Group 2 has a significantly different shape than groups 3 and 4 taken together for both behaviors. Finally, groups 3 and 4 had significantly different shapes during both station holding and swimming (see Table 1, Fig. 5). Discussion Sculpin pectoral fin function This study compared the function of the pectoral fin during two behaviors that place different functional demands on the fin, station holding and swimming. We have described morphological regionalization of the pectoral fin into dorsal and ventral regions. We have demonstrated that the fin rays in each region show consistent differences in curvature regardless of behavior. This suggests that the regions of the fin are functionally differentiated. We hypothesize that this differentiation allows this species to perform a broad range of behaviors necessary for a benthic existence. The rays with the highest curvature are those that routinely come into contact with the substrate, regardless of behavior. The ventral fin rays routinely interact with an unpredictable substrate to help increase friction and maintain station (Webb, 1989). They are also used to help the fish grip the substrate in the transition from swimming to station holding (Webb, 1989). Each of these behaviors requires flexibility and individual control of the fin rays. Therefore, it is not surprising that ventral fin rays exhibited the highest curvature and variation in magnitude of curvature between station holding and swimming. The two most dorsal rays, unexpectedly, were also relatively highly curved. This may be important for the role of these two most dorsal rays as the leading edge of the fin during swimming. During swimming, the most dorsal rays are convex into flow during swimming. The curvature of these rays may help stabilize the fin during swimming. The middle rays had the lowest overall curvature. This may reflect the need for stiffness or stability rather than flexibility. This stability is likely important for swimming but also plays a role during station holding in positioning the fin in such a way as to help streamline the profile of the fish in flow (Denny, 1988; Webb, 1989). Comparative fin ray curvature Despite considerable research on pectoral fin function in fishes (e.g. Walker & Westneat, 2002; Westneat et al., 2004; Drucker et al., 2006; Lauder & Madden, 2007), only one other study has measured fin ray curvature during locomotion (Standen & Lauder, 2005). In that study, the curvature of the median fin rays and fin shape was examined over a range of swim speeds and during maneuvering in bluegill sunfish. We compared our results with those from that study to investigate the range of variation in fin ray curvature and function in ray-finned fishes. There are broad similarities in how both species use their individual fin rays during locomotion. First, bluegill sunfish 6 Journal of Zoology ]] (2008) 1 9 c 2008 The Authors. Journal compilation c 2008 The Zoological Society of London

7 N. K. Taft, G. V. Lauder and P. G. A. Madden Functional regionalization of the pectoral fin control median fin shape primarily by changing the relative positions of the fin rays. Changes in curvature of rays are used to fine tune fin shape. Relative fin ray position is also used by longhorn sculpin to significantly alter pectoral fin shape during swimming versus substrate contact. Second, both species show evidence of fine muscular control over the curvature of individual fin rays. This is not surprising considering the general similarity in both species of fin ray morphology and the muscular mechanisms controlling curvature of individual fin rays (Geerlink & Videler, 1987). However, there are also important differences between the species. In the study of bluegill sunfish, Standen & Lauder (2005) found that individual fin rays were modestly curved, with curvature values on the order of 0.05 mm 1. The curvature of individual fin rays in the longhorn sculpin during slow swimming is more pronounced. At slow swim speeds, the maximum curvature of the fin rays is double that for bluegill sunfish swimming at comparable speeds (under 1TLs 1 ), and maximal curvature values for sculpin were nearly five times those of bluegill. Pectoral fin posture during slow swimming in sculpin is static; the fins do not oscillate. Greater curvatures of individual fin rays may not be necessary for bluegill, which change fin shape throughout a dynamic oscillation cycle. Both species show higher curvature during non-steady swimming behaviors. However, the difference in curvature between station holding and swimming in sculpin is much larger than that between maneuvering and swimming in the bluegill. There is also much more intra-fin variation in curvature in sculpin than was found in the median fins of bluegill sunfish. Finally, there were no consistent patterns of relative curvature among the individual fin rays of bluegill sunfish like those for longhorn sculpin. It is unclear whether these differences are due to differences between median and paired pectoral fins, or whether this is a small part of the large unexplored interspecies variation in the properties of fin ray function. Comparative pectoral fin function Our study describes a non-oscillating, steady pectoral fin posture during swimming for the longhorn sculpin. Pectoral fin posture of the longhorn sculpin during swimming superficially resembles that of a basal actinopterygian fish, the white sturgeon (Wilga & Lauder, 1999). Both species are negatively buoyant, benthic species that swim near the substrate. Superficially similar fin posture is achieved despite significant differences in pectoral fin structure. The relatively ventral location and horizontal insertion of the pectoral fins in sturgeon leads to a more natural horizontal positioning of the pectoral fins. Sculpins have more dorsally positioned, vertically inserted pectoral fins. Therefore, they undergo a complex folding behavior to orient the fin in this laterally extended posture during swimming (see Fig. 6). What is the function of the extended pectoral fins during swimming? It was hypothesized that in sturgeons, the pectoral fins were used for generating lift to counteract their negative buoyancy (Aleev, 1969). It has since been shown through high-speed video and particle image velocimetry (a) (b) COM = 33 % TL COM = 38 % TL COM= Center of Mass Figure 6 Lateral view line drawing of (a) longhorn sculpin and (b) sturgeon pectoral fin posture during swimming. These drawings are not drawn to scale; both fish have been drawn to the same total length. The center of mass of each fish is represented by an open circle, and the pectoral fins are outlined in grey. Note in the sculpin 1) the relatively anterior position of the center of mass, 2) the larger relative size of the pectoral fin and 3) the center of mass located directly above the posterior insertion of the pectoral fin. (PIV) analysis that in sturgeon the angle of the body is primarily responsible for lift during steady horizontal swimming (Wilga & Lauder, 1999). Changing the shape and angle of the pectoral fins during swimming does not directly generate lift. Rather, the pectoral fins aid in maneuvering the body during changes in position in the water column (Wilga & Lauder, 1999). In sculpin, the body is not angled, but parallel to the direction of flow (N. K. Taft, pers. obs.). There are other notable differences in the morphology and behavior between sculpins and sturgeons that support this hypothesis. First, the center of mass of sculpin is located anterior (33% total length) to that of sturgeon (38% total length) (N. K. Taft, pers. obs.) (see Fig. 6). More importantly, the center of mass in the longhorn sculpin is located almost directly over the center of the extended pectoral fin during swimming. In sturgeon the pectoral fin is located well anterior to the center of mass. Second, the pectoral fins of sculpins are longer and have a larger area relative to total body length than sturgeon. Finally, there is little to no muscle activity in the pectoral muscles during swimming to hold position in sturgeon (Wilga & Lauder, 1999). We have not yet collected data on muscle activity in sculpins but hypothesize that the pectoral fin musculature is actively involved in holding the folded fin in place during steady swimming. For these reasons, we hypothesize that sculpin are actively folding their broad pectoral fins into an extended posture to generate lift with their pectoral fins to counteract their negative buoyancy, not using the ventral body surface as do sturgeons. To further explore this idea, we conducted a preliminary analysis of the angle of attack of the pectoral fins relative to the horizontal body position (parallel to the flow) of the swimming fish in our analysis, two to six bouts per individual. We drew a chord line from the midpoint of the leading Journal of Zoology ]] (2008) 1 9 c 2008 The Authors. Journal compilation c 2008 The Zoological Society of London 7

8 Functional regionalization of the pectoral fin N. K. Taft, G. V. Lauder and P. G. A. Madden edge fin ray to the midpoint of the trailing edge of the fin. Angle of attack is the angle between this chord line and the parallel direction of the flow. Angle of attack during swimming ranged from 1.2 to These angles are within the range of angles, ideally 2 81, that could be used to produce lift during horizontal flight in aircraft (Kermode, 1996; Wilga & Lauder, 1999). Further work using PIV analysis is needed to support or refute this hypothesis. The pectoral fins of longhorn sculpin are flexible, broad and paddle shaped, which suggests that they are descended from fish that used their pectoral fins for a rowing form of propulsion (Walker & Westneat, 2002). In fact, a recent molecular phylogeny places the stickleback, an extreme rower (Walker & Westneat, 2002), basal to the clade including the cottoid fishes and their closest relatives (Smith & Wheeler, 2004). A flapping of the pectoral fins used by sculpins when moving very short distances along the substrate resembles the rowing motions used by sticklebacks. It is possible that the folding behavior used by sculpins to form the extended fin conformation during swimming is a modification of the rowing behavior of their ancestors. Understanding of pectoral fin function in teleost fishes thus far has focused primarily on propulsion or maneuvering during swimming in percomorph fishes that are not benthic (Geerlink, 1983, 1987; Gibb, Jayne & Lauder, 1994; Walker & Westneat, 1997, 2002; Drucker & Lauder, 2002, 2003; Westneat et al., 2004; Thorsen & Westneat, 2005; Drucker et al., 2006). Benthic fishes often use their pectoral fins for the competing functional demands of station holding and swimming. We propose that the pectoral fins of one benthic species, the longhorn sculpin, are morphologically and functionally specialized to meet the competing demands of station holding and swimming. Acknowledgments We would like the thank Erik Fel Dotto and the staff at Normandeau Associates, Hampton, NH, for aid in obtaining fish for our study. We thank Dr Steve McCormick, Mike O Dea, Dr Erika Henyey Parker and Brian Kynard for providing facilities and fish care at Conte Anadromous Fish Laboratory, Turners Falls, MA. We thank Emily Standen for help in calibrating our video sequences. We thank Benjamin Taft for MATLAB advice and comments on drafts of the paper. We thank Dr Gary Gillis of Mount Holyoke College, South Hadley, MA, for helpful discussions about the paper. We thank Dr Beth Brainerd for critical resources and support during the early stages of this project. This work was supported by an ONR-MURI Grant N on fish pectoral fin function, monitored by Dr Thomas McKenna and initiated by Dr Promode Bandyopadhyay, and by NSF grant IBN to G.V.L. References Alben, S., Madden, P.G. & Lauder, G.V. (2007). The mechanics of active fin-shape control in ray-finned fishes. J. Roy. Soc. 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