J_ID: JMOR Wiley Ed. Ref. No.: 1697 Customer A_ID: JMOR10551 Date: 15-JUNE-07 Stage: I Page: 1

JOURNAL OF MORPHOLOGY 00:000–000 (2007)

1 61 2 62 3 63 4 Functional Morphology of the Sonic Apparatus in the 64 5 65 6 Fawn Cusk-eel Lepophidium profundorum (Gill, 1863) 66 7 67 8 Michael L. Fine,1* Hsung Lin,1 Brian B. Nguyen,1 Rodney A. Rountree,2 68 9 Timothy M. Cameron,3 and Eric Parmentier4 69 10 70 11 1 Department of Biology, Virginia Commonwealth University, Richmond, Virginia 23284-2012 71 12 2 72 Marine Ecology and Technology Applications, 23 Joshua Lane, Waquoit, Massachusetts 02536 13 3 73 Department of Mechanical Engineering, Kettering University, Flint, Michigan 48504 14 4 74 Laboratoire de Morphologie Fonctionelle et Evolutive, Universite´ de Lie`ge, B-4000 Lie`ge, Belgium 15 75 16 76 17 ABSTRACT Recent reports of high frequency sound man, mormyrids, gurnards and searobins), the production by cusk-eels cannot be explained adequately 77 18 muscle contraction rate sets the fundamental fre- 78 by known mechanisms, i.e., a forced response driven by quency (Skoglund, 1961; Crawford and Huang, 19 fast sonic muscles on the swimbladder. Time to complete 79 20 1999; Bass and McKibben, 2003; Amorim and 80 a contraction-relaxation cycle places a ceiling on fre- Hawkins, 2005); i.e., simultaneous contraction of 21 quency and is unlikely to explain sounds with dominant 81 22 frequencies above 1 kHz. We investigated sonic morphol- paired sonic muscles at 200 Hz will drive a har- 82 23 ogy in the fawn cusk-eel Lepophidium profundorum to monic sound with a fundamental frequency of 200 83 24 determine morphology potentially associated with high Hz. The northern searobin alternates muscle con- 84 25 frequency sound production and quantified development traction so that the fundamental frequency is dou- 85 26 and sexual dimorphism of sonic structures. Unlike other ble the rate of individual contraction (Bass and 86 27 sonic systems in fishes in which muscle relaxation is Baker, 1991; Connaughton, 2004). More commonly, caused by internal pressure or swimbladder elasticity, 87 28 fish sounds are produced as a series of short-dura- 88 this system utilizes antagonistic pairs of muscles: ven- tion wide-band pulses (Winn, 1964). In weakfish 29 tral and intermediate muscles pull the winglike process 89 30 (family Sciaenidae), each sound pulse is driven by 90 and swimbladder forward and pivot the neural arch a single muscle twitch, and the dominant fre- 31 (neural rocker) above the first vertebra backward. This 91 32 action stretches a fenestra in the swimbladder wall and quency appears to be determined by timing char- 92 33 imparts strain energy to epineural ribs, tendons and lig- acteristics of the sonic muscle twitch rather than 93 34 aments connected to the anterior swimbladder. Rela- bladder resonance (Connaughton et al., 2002) sug- 94 35 tively short antagonistic dorsal and dorsomedial muscles gesting a similar mechanism to multicontraction 95 36 pull on the neural rocker, releasing strain energy, and tonal sounds. Rather than waiting for the contrac- 96 37 use a lever advantage to restore the winglike process tion of a muscle antagonist, muscle relaxation and and swimbladder to their resting position. Sonic compo- 97 38 hence the relaxation component of a twitch sound 98 nents grow isometrically and are typically larger in (Fine et al., 2001) is caused by bladder elasticity or 39 males although the tiny intermediate muscles are larger 99 40 pressure built up in the bladder by contraction of 100 in females. Although external morphology is relatively sonic muscles. Dispensing with antagonist contrac- 41 conservative in ophidiids, sonic morphology is extremely 101 42 variable within the family. J. Morphol. 000:000–000, tion removes the inertia that is otherwise involved 102 in a change of muscle direction necessary to com- 43 2007. Ó 2007 Wiley-Liss, Inc. 103 44 plete a sound cycle. Therefore, the timing of the 104 45 KEY WORDS: sonic muscle; Ophidiiformes; swimbladder; muscle contraction–relaxation cycle typically pla- 105 46 sound production; antagonistic muscles; acoustic commu- ces a ceiling on the maximum fundamental in lon- 106 47 nication; pivot joint ger-duration tonal sounds or dominant frequency 107 48 in single-twitch sounds. 108 49 Most fishes that use sonic swimbladder muscles 109 50 The frequency spectrum of fish sounds produced for sound production vocalize at relatively low fre- 110 51 by swimbladder vibration is determined as a forced quencies that fit the forced-twitch model. For 111 52 response to sonic muscle contraction and swim- example, sonic muscles in the oyster toadfish can 112 53 bladder properties (Sprague, 2000; Fine et al., 113 54 2001, 2004). The requirement for sonic muscles to 114 55 drive each sound cycle has selected for extreme *Correspondence to: Michael L. Fine, Department of Biology, 115 56 speed (Fine et al., 2001), and fish sonic swimblad- Virginia Commonwealth University, Richmond, VA 23284-2012. 116 57 der muscles are considered the fastest muscles in E-mail: mfi[email protected] 117 58 118 vertebrates (Tavolga, 1964; Rome and Linstedt, Published online 00 Month 2007 in 59 1998; Ladich and Fine, 2006). In fishes that make Wiley InterScience (www. interscience.wiley.com) 119 60 long duration tonal sounds (e.g., toadfish, midship- DOI: 10.1002/jmor.10551 120

Ó 2007 WILEY-LISS, INC.

ID: vasanss Date: 15/6/07 Time: 15:48 Path: J:/Production/JMOR/Vol00000/070042/3B2/C2JMOR070042 J_ID: JMOR Wiley Ed. Ref. No.: 1697 Customer A_ID: JMOR10551 Date: 15-JUNE-07 Stage: I Page: 2

2 M.L. FINE ET AL. 121 twitch sounds can have higher dominant frequen- 181 122 cies, and the maximum for the weakfish Cynoscion 182 123 regalis is above 500 Hz (Connaughton et al., 2002). 183 124 Note that high frequency components in fish 184 125 sounds (e.g., those above the peak frequency) rep- 185 126 resent higher order vibrations of the swimbladder 186 127 and not the driving frequency. In many cases, 187 128 these high frequency components may be above 188 129 the fish’s auditory range and therefore irrelevant 189 130 to communication (Ladich and Fine, 2006). 190 131 Ophidiids, the dominant group of benthic deep- 191 132 sea fishes in both numbers and species in tropical 192 133 and subtropical areas (Howes, 1992; Nielsen et al., 193 134 1999; Music personal communication), have swim- 194 135 bladder muscles, implicating them in sound pro- 195 136 duction (Marshall, 1967). Recent descriptions of 196 137 the sounds produced by a shallow-water ophidiid, 197 138 Ophidion marginatum, indicate a dominant fre- 198 139 quency above 1 kHz (Mann et al., 1997; Perkins, 199 140 2001; Sprague and Luczkovich, 2001; Rountree 200 141 and Bowers-Altman, 2002). This frequency is too 201 142 high to be explained by the twitch model because 202 143 no vertebrate muscle is known to complete a 203 144 twitch in less than 1 ms. We examined the sonic 204 145 anatomy underlying potentially high frequency 205 146 sound production in the fawn cusk-eel Lepophi- 206 147 dium profundorum, a species that lives on the 207 148 outer continental shelf in the Northwest Atlantic 208 149 Ocean (Collette and Klein-MacPhee, 2002) and 209 150 whose sounds have not been recorded. Although 210 151 direct evidence is lacking, we are proceeding under 211 152 the hypothesis that other ophidiids, but not related 212 153 carapids (Parmentier et al., 2006b), likewise pro- 213 154 duce high frequency sounds. Several previous 214 155 studies in ophidiids have clarified parts of the 215 156 mechanism and indicate considerable variability 216 157 within the sonic anatomy of the family (Rose, 217 158 1961; Courtenay, 1971; Carter and Musick, 1985; 218 159 Howes, 1992; Casadevall et al., 1996; Parmentier 219 160 et al., 2006a). These studies have noted sexual 220 161 dimorphism in sonic structures, and the present 221 162 study quantifies sexual differences for the first 222 163 time. 223 164 224 165 225 166 MATERIALS AND METHODS 226 167 227 168 Fawn cusk-eels Lepophidium profundorum (Gill, 1863) were Fig. 1. A: Relationship of weight to length for combined 228 169 captured by otter trawl and frozen aboard Albatross IV cruises. males and females in Lepophidium profundorum: Y 5 Fish were collected from Cape Hatteras to the Gulf of Maine at 229 0.01316X 2 170 1.116e , r 5 0.90. B: Relationship of skull weight to fish depths of about 50 fm from spring (March and April) and fall 230 2 171 weight: Males: Y 5264.91 1 21.72 X, r 5 0.80, Females: (September and October) bottom trawl surveys in 2001, 2002, 231 2 172 231.51 1 17.74X, r 5 0.84. C: Relationship of spine length to and 2004. 232 total length for combined males and females: Y 5 1.041 1 Specimens were weighed to 0.1 g and measured for total 173 2 233 0.02118X, r 5 0.60. length (TL) to the nearest millimeter, and gonads were exposed 174 to determine fish sex. Fish were dissected to expose muscles 234 175 attached to the swimbladder or to processes that connect to the 235 176 follow an electrical stimulus at 400 Hz without tet- bladder, and the origin and insertion of these muscles were 236 177 any (Fine et al., 2001) although the highest funda- described. We measured muscle length between the origin and 237 178 insertion and length of the tendons protruding from the ventral mental frequencies of toadfish recorded in nature muscle. Muscles (the right muscle of each pair) were weighed in 238 179 approach 300 Hz (Fine, 1978; Thorson and Fine, milligrams after soaking in 0.9% NaCl for 5 min and blotting to 239 180 2002; Remage-Healey and Bass, 2005). Single- ensure uniform hydration. Swimbladder length and weight 240

Journal of Morphology DOI 10.1002/jmor

ID: vasanss Date: 15/6/07 Time: 15:48 Path: J:/Production/JMOR/Vol00000/070042/3B2/C2JMOR070042 J_ID: JMOR Wiley Ed. Ref. No.: 1697 Customer A_ID: JMOR10551 Date: 15-JUNE-07 Stage: I Page: 3

SONIC MORPHOLOGY IN LEPOPHIDIUM PROFUNDORUM 3 241 301 242 302 243 303 244 304 245 305 246 306 247 307 248 308 249 309 250 310 251 311 252 312 253 313 254 314 255 315 256 316 257 317 258 318 259 319 260 320 261 321 262 322 263 Fig. 2. Dorsal and ventral 323 view of vertebrae I–V and epi- 264 neural ribs in male and female 324 265 Lepophidium profundorum. 325 266 326 267 327 268 328 269 were also measured. Dissected specimens were placed in hot the snout, which is not visible externally, increased 329 270 water with soap to facilitate tissue removal to expose the skele- linearly with fish size with no sexual difference 330 ton. We measured the length of the rostral spine, the dry 2 271 weight of the neurocranium (hereafter referred to as the skull) (Fig. 1C). The combined r value (0.60) was fairly 331 272 and the length, height, and weight of the winglike process and low because some spines were broken despite 332 273 weight of the ‘‘neural rocker.’’ The neural rocker and winglike being housed within tissue. Although likely defen- 333 274 process were broken at a suture allowing us to weigh the two sive, spine function is unknown, and these obser- 334 components individually. vations appear to rule out a courtship function or 275 Quantitative data from the skeleton, swimbladder, and sonic 335 276 muscles were regressed against fish size (weight and total a contribution to sexual dimorphism in head 336 277 length), and sexual differences were determined by analysis of weight. 337 278 covariance. We used regressions to calculate adjusted means to 338 279 compare male and female characters for a medium-sized indi- vidual (225 mm TL and 25 g). 339 280 Sonic Mechanism 340 281 Skeleton. The first five vertebrae bear epineu- 341 282 ral ribs of different sizes (Figs. 2, 6, and 7). The 342 RESULTS F2 283 first vertebra bears a large complex process con- 343 284 Fish ranged from 130 to 274 mm TL and sisting of an expanded rib, the winglike process, 344 285 included 36 females and 29 males. Size distribu- and a neural arch with two small median articula- 345 286 tions were similar for both sexes, and males and tion heads that fit within depressions on the side 346 287 females were not distinguishable externally. They of the first vertebra (Figs. 2 and 3). These two 347F3 288 had equivalent length–weight regressions, which attachments confine movement to a single plane: 348 289 were therefore combined into a single regression the neural arch and spine pivot (rock back and 349 0.01316 TL 2 290F1 (Y 5 1.116e , r 5 0.90) (Fig. 1A, Table 2). forth) in the anteroposterior direction. We refer to 350 291 Skull weight increased linearly with fish weight this structure as the neural rocker to distinguish 351 292 (male r2 5 0.84, female r2 5 0.80) (Fig. 1B, Ta- it from the rocker bone found in the anterior 352 293 ble 2). Although there was considerable overlap swimbladder wall in other ophidiids (Rose, 1961; 353 294 between males and females, skulls were heavier Casadevall et al., 1996). The neural rocker is 354 295 in males than in females (F1,60 5 6.1988, P 5 larger in males (Tables 1 and 2, Fig. 8) and has 355T1, T2 296 0.0156). Notably, a keel on the midline of the cau- expanded lateral shoulders compared to a more 356 297 dal part of the parasphenoid, which separates the rounded contour in females (Figs. 2 and 3). The 357 298 right and left ventral sonic muscles (see below), winglike process is fused to the anterolateral base 358 299 was sufficiently deeper in males that this charac- of the neural rocker at a suture, and the two can 359 300 ter can be used to determine fish sex. The spine on be removed as a single structure. The medial half 360

Journal of Morphology DOI 10.1002/jmor

ID: vasanss Date: 15/6/07 Time: 15:48 Path: J:/Production/JMOR/Vol00000/070042/3B2/C2JMOR070042 J_ID: JMOR Wiley Ed. Ref. No.: 1697 Customer A_ID: JMOR10551 Date: 15-JUNE-07 Stage: I Page: 4

4 M.L. FINE ET AL. 361 (Fig. 2). The width of the winglike process is 421 362 slightly wider in males than in females and consid- 422 363 erably longer in males because of the distal tip 423 364 (Figs. 2 and 8). A ligament on the ventrolateral 424 365 surface of the winglike process (SWB ligament 1a) 425 366 connects to the anterior face of the swimbladder 426 367 (SWB) (Figs. 2, 5, and 7). 427 368 The remaining epineural ribs (EP2–5) have a 428 369 single slender articulation head that would allow 429 370 them to move in different directions except that 430 371 movement is restricted by their attachments, 431 372 which forms a scaffold over the anterior bladder 432 373 (Figs. 2 and 7). The winglike process connects to 433 374 EP2 by a ligament (SWB ligament 1b), and the tip 434 375 of EP2 bears a ligament (SWB ligament 2) that 435 376 connects to the swimbladder (Fig. 7). EP3 is thin 436 377 proximally and becomes broader laterally binding 437 378 to the bladder with connective tissue. The proxi- 438 379 mal part of EP3 connects to the osseous plate on 439 380 vertebra 4, which should restrict forward move- 440 381 ment of the rib and stabilize the bladder. The osse- 441 382 ous plate is larger with a greater lateral extension 442 383 in males than females (Table 2). A smaller but 443 384 similar structure is present on vertebra 5. 444 385 Swimbladder morphology. The swimbladder 445 386 is a slender sac consisting of a single chamber, 446 387 which increases in girth from the anterior end for 447 388 a short distance before gradually tapering. The 448 389 bladder ends in a tail that is longer in females 449 390 than in males (Figs. 4 and 5C). The bladder lies 450F4, F5 391 under the first through twelfth vertebrae and is 451 392 tightly coupled to the vertebral column through 452 393 the ninth vertebra. Again note particularly the 453 394 broad attachment site on the osseous plate on the 454 395 fourth and to a lesser extent on the fifth vertebra 455 396 (Figs. 2 and 7). Interestingly, the posterior portion 456 397 of the bladder is less closely attached but held to 457 398 the 10th through 12th vertebrae by three strong 458 399 string-like bands of connective tissue (Fig. 4C). 459 400 The bladder has a similar length in males and 460 401 females but is considerably heavier in males 461 402 (Tables 1 and 2, Fig. 9). 462 403 The bladder may be divided into three regions. 463 404 The anterior region is notably thickened and is 464 405 the attachment site for sonic muscle ligaments 465 406 (described above) and tendons (described under 466 407 muscles). The second region, termed the swimblad- 467 408 der fenestra in ophidiiform fishes (Howes, 1992), is 468 409 thin and transparent without an outer collagenous 469 410 Fig. 3. Neural rocker (first neural arch), winglike process covering (Fig. 5A,B). The final region, the remain- 470 411 (WLP) and pivot joint in Lepophidium profundorum. Note the der of the bladder, is tightly coupled to the verte- 471 broad shoulders on the neural rocker in A, the expanded tip of 412 the WLP and the projections of the pivot joint in B, which fit bral column, and begins at epineural rib 3 (EP3). 472 413 into the recesses in the vertebra in C. Scale bar 5 1 mm. The fenestra in males covers three-fourths of the 473 414 swimbladder circumference and is larger dorsally 474 415 tapering around the bladder sides (Fig. 5A). In 475 416 of the winglike process is concave and narrows lat- females, the smaller fenestra is restricted to the 476 417 erally to a ridge with a crest on the lateral margin. dorsal surface. The anterior lip of the fenestra 477 418 The crest is deeper in males than in females, and (ALF) is notably thickened and is the insertion 478 419 the expanded tip of the winglike process is nar- site of SWB ligament 2. The fenestra is more flexi- 479 420 rower and more pointed in males than in females ble than other bladder tissue and permits muscle 480

Journal of Morphology DOI 10.1002/jmor

ID: vasanss Date: 15/6/07 Time: 15:48 Path: J:/Production/JMOR/Vol00000/070042/3B2/C2JMOR070042 J_ID: JMOR Wiley Ed. Ref. No.: 1697 Customer A_ID: JMOR10551 Date: 15-JUNE-07 Stage: I Page: 5

SONIC MORPHOLOGY IN LEPOPHIDIUM PROFUNDORUM 5 481 TABLE 1. Summary of sexually dimorphic characters in the sonic system of Lepophidium profudorum 541 482 Character Male Female 542 483 543 484 Ventral muscle Heavier and thicker Lighter and thinner 544 485 Intermediate muscle Lighter and narrow Heavier and wide 545 Dorsal muscle Heavier and thicker Lighter and thinner 486 Parasphenoid keel Wide Narrow 546 487 Posterior tip of the swim bladder Short Elongated 547 488 Swim bladder fenestra Wide and long Narrow and short 548 489 Ligament between EP1 and EP2 Thin Large, ligament runs to EP3 549 Ventral plate on the 4th vertebra Large Small 490 Wing-like process Elongated posterior tip Shorter tip 550 491 Neural rocker Larger with flattened dorsal Thin and rounded 551 492 aspect and lateral shoulder 552 493 553 494 554 495 555 496 attachments to displace the anterior wall of the Ventral muscle. The ventral muscles originate 556 497 bladder (region 1). Dorsally, the region just caudal broadly on the flattened parasphenoid and are sep- 557 498 to the posterior edge of the fenestra attaches to arated by a vertical keel, which is more extensive 558 499 EP3, and, as stated previously, the motion of this in males than females (Figs. 6 and 7). These 559 500 rib is severely restricted by ligament EP3–EP4, muscles end in a long tendon that bifurcates. The 560 501 which connects the proximal end of EP3 to the os- straight portion runs directly to its insertion on 561 502 seous plate on vertebra 4. This connection, as well the midportion of the ridge crest on the ventral 562 503 as the tight coupling of the dorsal swimbladder winglike process (Figs. 4, 6, and 7). The ventral 563 504 wall to the vertebral column, will hold the poste- muscle tendon branches at a right angle, forming 564 505 rior bladder relatively rigid during sonic muscle an intermuscular tendon that connects to the op- 565 506 contraction. posite ventral muscle tendon after running 566 507 Sonic muscles. The fawn cusk-eel has four through the thickened anterior wall of the swim- 567 508 pairs of sonic muscles (ventral, intermediate, dor- bladder (Figs. 4B and 5A). Thus, the ventral mus- 568 509 sal and dorsomedial), all of which insert on the cle forms an indirect lateral and a direct medial 569 510 swimbladder or skeletal elements that move the attachment to the swimbladder. 570 F6,511 F7 swimbladder (Figs. 4, 5A, 6, and 7). These muscles Intermediate muscle. The intermediate mus- 571 512 have been given various names in other ophidiids; cle originates on a protrusion situated behind the 572 513 for instance, the ventral muscles have been foramen of the vagal nerve on the anterior part of 573 514 referred to as M1 (Rose, 1961), primary sonic mus- the basioccipital (Fig. 6). The muscle is narrow 574 515 cle (Courtenay and McKittrick, 1970), ventrolat- and runs beneath Baudelot’s ligament in males, 575 516 eral and ventromedial sonic muscles (Carter and whereas in females it is wider and surrounds 576 517 Musick, 1985), and anterolateral segment of the the ligament. The insertion of the intermediate 577 518 epaxial muscle (Howes, 1992). Hopefully the termi- muscles, medial to the insertion of the ventral 578 519 nology used here and in Parmentier et al. (2006a) muscles, is on a curved ridge that travels down 579 520 will become standard. the ventral side of the winglike process. The ridge 580 521 581 522 582 523 TABLE 2. Sexual dimorphism of sonic structures in Lepophidium profundorum 583 524 584 525 Structure Male Female Probability 585 526 Ventral muscle L (mm) 13.6 11.8 <0.0001 586 527 Ventral muscle Wt (mg) 78.0 54.0 <0.0001 587 528 Intermediate muscle L (mm) 7.8 7.6 NS 588 529 Intermediate muscle Wt (mg) 6.7 13.5 <0.0001 589 Dorsal muscle L (mm) 10.9 9.4 <0.0001 530 Dorsal muscle Wt (mg) 80.0 38.0 <0.0001 590 531 Ventral muscle tendon L, (mm) 3.1 2.2 0.038 591 532 Intermuscular tendon L (mm) 2.8 3.1 NS 592 533 WLP width (mm) 2.5 2.2 0.0028 593 534 WLP length (mm) 7.4 5.9 0.0018 594 WLP weight (mg) 14.9 7.4 <0.0001 535 Neural rocker Wt (mg) 6.7 3.6 0.0003 595 536 Swimbladder L (mm) 31.0 31.0 NS 596 537 Swimbladder Wt (mg) 511.0 363.0 0.0006 597 538 Adjusted means were calculated for a 225 mm TL or 25 mg fish using regressions for males and 598 539 females; Probability values were taken from analysis of covariance; In many cases (see graphs), the 599 540 slopes were equal in which case the P value indicates significance of elevation. 600

Journal of Morphology DOI 10.1002/jmor

ID: vasanss Date: 15/6/07 Time: 15:48 Path: J:/Production/JMOR/Vol00000/070042/3B2/C2JMOR070042 J_ID: JMOR Wiley Ed. Ref. No.: 1697 Customer A_ID: JMOR10551 Date: 15-JUNE-07 Stage: I Page: 6

6 M.L. FINE ET AL. 601 forms a posterior border of a concave surface on 661 602 the process. 662 603 Dorsal muscle. The dorsal muscle originates on 663 604 the epiotic, exoccipital, and the anterior portion of 664 605 the supraoccipital crest (Fig. 6A,B) and extends to 665 606 the lateral posterior portion of the dorsal surface of 666 607 the neural rocker (Figs. 6 and 7). A medial dorso- 667 608 ventrally compressed dorsomedial muscle (DMm), 668 609 described here for the first time, connects the pos- 669 610 terior tip of the supraoccipital to the apex of the 670 611 neural rocker. 671 612 672 613 673 614 674 Relative Growth and Sexual Dimorphism 615 675 616 The dorsal, intermediate, and ventral sonic 676 617 muscles exhibited a linear increase in length and 677 618 weight with fish size and were sexually dimorphic 678 619 (Tables 1 and 2, Fig. 10). The dorsal and ventral 679 620 muscles were larger in males, but the intermediate 680 621 muscle was larger in females. The dorsal muscle 681 622 in males had an adjusted mean weight of 80 mg 682 623 (calculated for a midsized 25 g, 225 mm TL fish), 683 624 the ventral muscle 78 mg, and the thin intermedi- 684 625 ate muscle was considerably lighter at 6.7 mg. 685 626 Comparable values in females were 38, 54, and 686 627 13.5 mg, respectively. Comparisons of the muscles 687 628 within each sex (Table 2) indicate that the ventral 688 629 muscle is longer than the dorsal muscle in both 689 630 sexes and heavier than the dorsal muscle in 690 631 females; in males the two muscles were compara- 691 632 ble in weight (P > 0.05). The intermediate muscles 692 633 were shorter and lighter than the other two in 693 634 both sexes. 694 635 Swimbladder lengths were similar in both sexes, 695 636 but bladders were heavier in males (Table 2, Fig. 696 637 9). The tendon of the ventral muscle was longer in 697 638 males, but intermuscular tendon length was simi- 698 639 lar in both sexes (Table 2, Fig. 9). Finally, the neu- 699 640 ral rocker was heavier in males as reflected in its 700 641 broader structure (Figs. 2 and 8), and the winglike 701 642 process was slightly wider, longer and therefore 702 643 considerably heavier in males than in females (Ta- 703 644 ble 2, Fig. 8). The increased length of the winglike 704F8 645 process accommodates the longer ventral muscle 705 646 and ventral muscle tendon in males. Since the 706 647 ventral tendon inserts laterally on the slender tip 707 648 of the winglike process, the longer ventral muscle 708 649 in males should impart a greater torque on the 709 650 winglike process, thereby increasing the movement 710 651 of the swimbladder during sound production. 711 652 The regression of dorsal muscle weight against 712 653 fish weight had a greater slope in males than in 713 654 females as did ventral muscle tendon length, neu- 714 655 Fig. 4. A: The swimbladder of Lepophidium profundorum. ral rocker weight, winglike process weight, and 715 B: The ventral muscles (VM) with the protruding ventral mus- 656 cle tendon (VMT) that attaches to the WLP, and the intermus- swimbladder weight (Figs. 8–10). However, muscle 716F9, F10 657 cular tendon (IMT) that enters the anterior wall of the bladder. length of all three sonic muscles and weights of 717 658 The anterior wall has been cut away to reveal the tendon. C: the ventral and intermediate muscles grew at an 718 659 Stringlike connective tissue attachments from vertebrae 10–12 equivalent rate in both sexes (slopes were not 719 660 to the posterior bladder. significantly different) although structures were 720

Journal of Morphology DOI 10.1002/jmor

ID: vasanss Date: 15/6/07 Time: 15:48 Path: J:/Production/JMOR/Vol00000/070042/3B2/C2JMOR070042 J_ID: JMOR Wiley Ed. Ref. No.: 1697 Customer A_ID: JMOR10551 Date: 15-JUNE-07 Stage: I Page: 7

SONIC MORPHOLOGY IN LEPOPHIDIUM PROFUNDORUM 7 721 781 722 782 723 783 724 784 725 785 726 786 727 787 728 788 729 789 730 790 731 791 732 792 733 793 734 794 735 795 736 796 737 797 738 798 739 799 740 800 741 801 742 802 743 803 744 804 745 Fig. 5. Sonic specializations 805 746 of the swimbladder in male and 806 747 female Lepophidium profundo- 807 748 rum. A: The intermuscular 808 tendon (IMT), swimbladder fe- 749 nestra, and anterior lip of the 809 750 fenestra (ALF). B: The attach- 810 751 ment of the ventral muscles 811 752 (VM) to the WLP, WLP attach- 812 753 ment to the bladder via tendon 813 L1a, and the side view of the 754 swimbladder fenestra in the 814 755 male but not in the female. C: 815 756 Swimbladder tail, which is lon- 816 757 ger in females than males. 817 758 818 759 819 760 820 761 larger in one sex (e.g. males except for the inter- DISCUSSION 821 762 mediate muscles), indicative of significant differen- 822 Knowledge of sound production in deep-sea 763 ces in elevations of the regressions. 823 fishes is circumstantial (Mann and Jarvis, 2004) 764 Function. Pulling on the ventral and interme- 824 765 diate muscles causes the winglike process to pivot and based mainly on anatomy, i.e., the presence of 825 766 forward thereby forcing the anterior surface of the sonic swimbladder muscles (Marshall, 1967). To 826 767 swimbladder forward and downward, and thus our knowledge, the striped cusk-eel Ophidion mar- 827 768 stretching the swimbladder fenestra (Fig. 7). This ginatum, which lives in shallow water, is the only 828 769 process is aided by a series of connections (swim- identified ophidiid whose sounds have been re- 829 770 bladder ligaments 1a, 1b, 2, and the intermuscu- corded (Mann et al., 1997; Perkins, 2001; Sprague 830 771 lar tendon). Therefore, contraction of the ventral and Luczkovich, 2001; Rountree and Bowers-Alt- 831 772 and intermediate muscles will place these ele- man, 2002), and its sound pulses have anoma- 832 773 ments under tension (Fig. 7). Motion of the wing- lously high peak frequencies exceeding 1 kHz. We 833 774 like process causes the neural rocker to pivot started our investigation into the sonic anatomy of 834 775 backward until it is pinned against the dorsal the fawn cusk-eel Lepophidium profundorum to 835 776 spine of the second vertebra, which therefore func- uncover anatomical features that might lead to 836 777 tions as a stop to ventral muscle contraction. Con- high frequency sound production. The discovery of 837 778 traction of the dorsal muscle antagonist pivots antagonistic muscle pairs was disconcerting, since 838 779 the neural rocker forward, restoring swimbladder a muscle antagonist must slow down one action 839 780 position. before starting another, thereby seemingly favor- 840

Journal of Morphology DOI 10.1002/jmor

ID: vasanss Date: 15/6/07 Time: 15:48 Path: J:/Production/JMOR/Vol00000/070042/3B2/C2JMOR070042 J_ID: JMOR Wiley Ed. Ref. No.: 1697 Customer A_ID: JMOR10551 Date: 15-JUNE-07 Stage: I Page: 8

8 M.L. FINE ET AL. 841 901 842 902 843 903 844 904 845 905 846 906 847 907 848 908 849 909 850 910 851 911 852 912 853 913 854 914 855 915 856 916 857 917 858 918 859 919 860 920 861 921 862 922 863 923 864 924 865 925 866 926 867 927 868 928 869 929 870 930 871 931 872 932 873 933 874 934 875 935 876 936 877 937 878 938 879 939 880 940 881 941 882 942 883 943 884 944 885 945 886 946 887 947 Fig. 6. Top: Drawing of the skull, first 888 5 vertebrae and epineural ribs in Lepo- 948 889 phidium profundorum. Middle: Drawing 949 890 of the ventral, intermediate, and dorsal 950 891 muscles superimposed on the skeleton. 951 892 Bottom: Micrograph of the sonic muscles. 952 893 953 894 954 895 ing lower rather than higher swimbladder vibra- nism of sound generation in cusk-eels would still 955 896 tion frequencies. require opposite movements of the muscle antago- 956 897 Swimbladder sounds typically result from forced nists to occur in less than 1 ms to produce a sound 957 898 responses to muscle contraction (Fine et al., 2001; with a dominant frequency above 1 kHz. Such 958 899 Connaughton et al., 2002; Connaughton, 2004; speed is unlikely for muscle contraction or motor 959 900 Fine et al., 2004). However, a typical fish mecha- neuron control. Another avenue for generating 960

Journal of Morphology DOI 10.1002/jmor

ID: vasanss Date: 15/6/07 Time: 15:49 Path: J:/Production/JMOR/Vol00000/070042/3B2/C2JMOR070042 J_ID: JMOR Wiley Ed. Ref. No.: 1697 Customer A_ID: JMOR10551 Date: 15-JUNE-07 Stage: I Page: 9

SONIC MORPHOLOGY IN LEPOPHIDIUM PROFUNDORUM 9 961 1021 962 1022 963 1023 964 1024 965 1025 966 1026 967 1027 968 1028 969 1029 970 1030 971 1031 C 972 1032 O 973 1033 L 974 1034 O 975 1035 R 976 1036 977 1037 978 1038 979 1039 980 1040 981 1041 982 1042 983 1043 984 1044 985 1045 986 1046 987 1047 988 1048 989 1049 990 1050 991 1051 992 1052 993 1053 994 1054 995 1055 996 1056 997 1057 998 Fig. 7. Top: Drawing of the 1058 999 skull and anterior vertebrae illus- 1059 1000 trating torque patterns of the ven- 1060 1001 tral, intermediate, and dorsal 1061 1002 muscles on the neural rocker and 1062 WLP. Bottom: Schematic diagram 1003 of the sonic apparatus including 1063 1004 skeletal elements, tendons, and 1064 1005 sonic muscles in male and female 1065 1006 Lepophidium profundorum. 1066 Arrows in the right figure illus- 1007 trate movements of ligaments, ten- 1067 1008 dons, and the swimbladder fenes- 1068 1009 tra during contraction of the ven- 1069 1010 tral and intermediate muscles. 1070 1011 1071 1012 1072 1013 1073 1014 sounds has been demonstrated in carapid fishes, mentier et al., 2006b). For comparison, toadfish 1074 1015 which are closely related to the ophidiids (Cour- sonic muscles require about 10 ms for a twitch and 1075 1016 tenay and McKittrick, 1970; Nielsen et al., 1999). can follow an electrical stimulus at 400 Hz (Sko- 1076 1017 Unlike all other sounds generated by fast sonic glund, 1961; Fine et al., 2001). Resonant frequency 1077 1018 swimbladder muscles, sounds in Carapus acus are calculations (Weston, 1967) for an underwater bub- 1078 1019 generated with slow muscles that require 490 ms ble with an equivalent radius to the swimbladder 1079 1020 for a twitch and that tetanize above 10 Hz (Par- in Carapus boraborensis predicted frequencies an 1080

Journal of Morphology DOI 10.1002/jmor

ID: vasanss Date: 15/6/07 Time: 15:49 Path: J:/Production/JMOR/Vol00000/070042/3B2/C2JMOR070042 J_ID: JMOR Wiley Ed. Ref. No.: 1697 Customer A_ID: JMOR10551 Date: 15-JUNE-07 Stage: I Page: 10

10 M.L. FINE ET AL. 1081 1141 1082 1142 1083 1143 1084 1144 1085 1145 1086 1146 1087 1147 1088 Fig. 8. Relationship of winglike 1148 1089 process (WLP) and neural rocker 1149 1090 to total length or weight in male 1150 1091 and female Lepophidium profundo- 1151 rum. A: WLP width to TL. Males: 1092 Y 520.1981 1 0.01183X, r2 5 1152 1093 0.60. Females: Y 520.4154 1 1153 1094 0.01171X, r2 5 0.70. B: WLP 1154 1095 length to TL. Males: Y 521.27 1 1155 0.0386X, r2 5 0.87. Females: Y 5 1096 2 1156 20.1673 1 0.02741X, r 5 0.88. C: 1097 WLP weight to fish weight. Males: 1157 1098 0.01183X, r2 5 0.60. Females: Y 5 1158 1099 20.4154 1 0.01171X, r2 5 0.70. 1159 1100 WLP length to TL. Males: Y 5 1160 21.27 1 0.0386X, r2 5 0.87. 1101 Females: Y 521.296 1 0.3471X, 1161 1102 r2 5 0.88. D: Neural rocker weight 1162 1103 to fish weight. Males Y 522.235 1163 1 0.3570X, r2 5 0.72. Females: Y 1104 2 1164 1105 520.04565 1 0.1465X, r 5 78. 1165 1106 1166 1107 1167 1108 octave higher than that produced by the fish (Par- lateral insertion. It is conceivable that residual 1168 1109 mentier et al., 2006b). Since the swimbladder of ventral and intermediate muscle contraction after 1169 1110 the fawn cusk-eel is larger than that of C. borabor- the stop increases tension on the winglike process, 1170 1111 ensis, generation of high frequency sounds by blad- tendons, and ligaments as if they were spring- 1171 1112 der resonance is unlikely. A swimbladder fenestra loaded. The intermediate muscles have larger 1172 1113 (Howes, 1992), which decouples sonic muscle- fibers than the ventral and dorsal muscles in 1173 1114 induced movement of the anterior swimbladder Ophidion barbatum (Parmentier et al., 2006a), 1174 1115 from the rest of the structure, occurs in both and it is therefore plausible that the intermediate 1175 1116 carapids and ophidiids. Therefore, it is parsimoni- muscles will be slower and maintain tension after 1176 1117 ous to assume that fawn cusk-eel sounds are also the stop. Further, we hypothesize that the 1177 1118 induced by slow muscles. Another parallel between extended thin tips of the male winglike process are 1178 1119 carapids and the fawn cusk-eel is the presence of an adaptation to store strain energy (Alexander, 1179 1120 modified ribs in close association with the swim- 2002). 1180 1121 bladder fenestra. In C. boraborensis, a broad modi- The ligament attaching the third epineural rib 1181 1122 fied rib, the swimbladder plate, is intimately con- to the osseus plate on vertebra 4 plus the intimate 1182 1123 nected to the fenestra, and Parmentier et al. attachments of the dorsal swimbladder to the ver- 1183 1124 (2006a) hypothesized that the plate is excited by tebral column isolates the posterior bladder from 1184 1125 the rapid return of the fenestra, which was muscle contractions. In fact, the system is 1185 1126 stretched and then released by sonic muscle con- designed to displace the anterior portion of the 1186 1127 traction; plate vibrations in turn were seen as swimbladder forward primarily by stretching the 1187 1128 driving the swimbladder and determining the fenestra. The complex bladder attachments of the 1188 1129 sound frequency. ventral muscles (winglike process laterally and 1189 1130 Although the carapid mechanism does not utilize intermuscular tendon medially) act as a stay to 1190 1131 antagonistic muscles, we see a number of parallels keep the front of the bladder from buckling, 1191 1132 in the sonic mechanism in the fawn cusk-eel. The thereby serving to transfer muscle work efficiently 1192 1133 cusk-eel’s ventral and intermediate muscles pull to bladder displacement. Swimbladder shape is 1193 1134 the swimbladder forward, pivoting the neural restored by shorter antagonistic dorsal and dorso- 1194 1135 rocker backward until it hits the neural arch of medial muscles that work indirectly by pulling the 1195 1136 the second vertebra, which should rapidly termi- neural rocker forward. Because of the pivot action 1196 1137 nate motion. The ventral muscles will be more and the longer winglike process, the dorsal 1197 1138 effective in deforming the swimbladder than the muscles enjoy a mechanical lever advantage (for 1198 1139 intermediate muscles because of their greater speed but not force) so that a short movement will 1199 1140 mass and length, greater tendon length, and more be translated into a longer motion of the swim- 1200

Journal of Morphology DOI 10.1002/jmor

ID: vasanss Date: 15/6/07 Time: 15:50 Path: J:/Production/JMOR/Vol00000/070042/3B2/C2JMOR070042 J_ID: JMOR Wiley Ed. Ref. No.: 1697 Customer A_ID: JMOR10551 Date: 15-JUNE-07 Stage: I Page: 11

SONIC MORPHOLOGY IN LEPOPHIDIUM PROFUNDORUM 11 1201 1261 1202 1262 1203 1263 1204 1264 1205 1265 1206 1266 1207 1267 1208 1268 1209 1269 1210 1270 1211 1271 1212 1272 1213 1273 1214 1274 1215 1275 1216 1276 1217 1277 1218 1278 1219 1279 1220 1280 1221 1281 1222 1282 1223 1283 1224 1284 1225 Fig. 9. Relationship of swimbladder length and weight to total length or weight and ventral muscle tendon and intermuscular 1285 1226 tendon length to total length in male and female Lepophidium profundorum. A: Swimbladder length to TL. Males: Y 5215.24 1 1286 0.2059X, r2 5 0.82. Females: 29.457 1 0.1803X, r2 5 0.89. B: Swimbladder weight to fish weight. Males: Y 5246.64 1 22.31X, r2 1227 5 0.84. Females: Y 5 10.96 1 14.06X, r2 5 0.79. C: Ventral muscle tendon length to TL. Males: Y 522.477 1 0.02492X, r2 5 1287 1228 0.43. Females: Y 520.4753 1 0.0119X, r2 5 0.31. D: Intermuscular tendon length to TL. Males: Y 521.057 1 0.01735X, r2 5 1288 1229 0.52. Females: Y 521.463 1 0.02017X, r2 5 0.63. 1289 1230 1290 1231 1291 1232 bladder. Measuring from the prongs that insert in ity (Bradbury and Vehrencamp, 1998), suggesting 1292 1233 the vertebra, the ratio of the height of the neural the flat surface of the bladder between the fenes- 1293 1234 rocker to the length of the winglike process in a tra and the tail is primarily responsible for radiat- 1294 1235 male is about 1:2.5. Therefore, a small forward ing sound. 1295 1236 movement of the rocker will exert a magnified dis- Pivot joints in mammals permit a circular rota- 1296 1237 placement of the bladder approximating that ratio. tion (Marieb and Mallatt, 2001), e.g., the proximal 1297 1238 However, the lever advantage of the dorsal radioulnar and alantoaxial joints in humans, 1298 1239 muscles results in a force disadvantage. Since con- which allow us respectively to rotate our forearm 1299 1240 traction of the dorsal muscles will release strain and our head from side to side. The attachment of 1300 1241 energy (Alexander, 2002) stored in the winglike the neural rocker to the first vertebra, a longitudi- 1301 1242 process, tendons and epineural rib 2 (Fig. 7), dor- nal pivot joint whose motion is restricted to the 1302 1243 sal muscle action should not require a great deal anterior–posterior plane, appears to be a new type 1303 1244 of force. The bladder should pop back rapidly, gen- of joint with low inertia and a stop that would 1304 1245 erating a rapid increase in pressure within the favor high speed cycling. 1305 1246 bladder. Note that the dorsal muscle in the striped Preliminary audiograms for the striped cusk-eel 1306 1247 cusk-eel undergoes a seasonal hypertrophy that Ophidion marginatum indicate it is an auditory 1307 1248 should facilitate bladder return (Courtenay, 1971). generalist with low frequency hearing (B. Casper 1308 1249 The bladder ends in a little tail, and similar tails and D. Mann, personal communication). They 1309 1250 are present in unrelated sciaenid fishes (Chao, found an upper auditory limit of 800 Hz using the 1310 1251 1978), suggesting convergent evolution. The wide auditory brainstem response. We therefore suggest 1311 1252 anterior end of the bladder will admit high veloc- that the cusk-eel sonic mechanism evolved to pro- 1312 1253 ities courtesy of the fenestra, and the taper down duce high sound pressure levels with slow muscles 1313 1254 to the more rigid posterior tail will concentrate the and that high frequency sound production was gen- 1314 1255 pressure of an acoustic wave and reflect it back to erated incidentally, basically an epiphenomenon. 1315 1256 the anterior end where it could potentially re- Therefore, only low frequency components of the 1316 1257 excite tendons and ligaments, evoking a multicycle sound spectrum, those below the peak frequency, are 1317 1258 pulse. The swimbladder tail will not be an effective likely to play a role in acoustic communication. 1318 1259 sound radiator because of its small surface area The phylogeny of ophidiiform fishes is poorly 1319 1260 and resistance to movement, i.e., low volume veloc- understood (Nielsen et al., 1999) and does not 1320

Journal of Morphology DOI 10.1002/jmor

ID: vasanss Date: 15/6/07 Time: 15:50 Path: J:/Production/JMOR/Vol00000/070042/3B2/C2JMOR070042 J_ID: JMOR Wiley Ed. Ref. No.: 1697 Customer A_ID: JMOR10551 Date: 15-JUNE-07 Stage: I Page: 12

12 M.L. FINE ET AL. 1321 1381 1322 1382 1323 1383 1324 1384 1325 1385 1326 1386 1327 1387 1328 1388 1329 1389 1330 1390 1331 1391 1332 Fig. 10. Relationship of dorsal, 1392 1333 intermediate, and ventral muscle 1393 length and weight to fish total 1334 length and weight in male and 1394 1335 female Lepophidium profundorum. 1395 1336 A: Dorsal muscle length to TL. 1396 1337 Males: Y 524.139 1 0.06668X, r2 1397 5 0.80. Females: Y 523.713 1 1338 2 0.05841X, r 5 0.78. B: Intermedi- 1398 1339 ate muscle length to TL. Males: Y 1399 1340 521.237 1 0.03907X, r2 5 0.64. 1400 1341 Females: Y 521.227 1 0.4011X, 1401 2 1342 r . C: Ventral muscle length to TL. 1402 Males: Y 522.219 1 0.07009X, r2 1343 5 0.75. Females: Y 523.641 1 1403 1344 0.06883X, r2 5 0.88. D: Dorsal 1404 1345 muscle weight to fish weight. 1405 1346 Males: 211.22 1 3.638X, r2 5 1406 0.80. Females: Y 526.373 1 1347 1.769X, r2 5 0.68. E: Intermediate 1407 1348 muscle weight to fish weight. 1408 1349 Males: Y 5 0.00995 1 0.2668X, r2 1409 1350 5 0.49. Females: Y 5 2.849 1 1410 2 1351 0.4243X, r 5 0.53. F: Ventral 1411 muscle weight to fish weight. 1352 Males: Y 5 6.986 1 2.836X, r2 5 1412 1353 0.54. Females: Y 526.197 1 1413 1354 2.392X, r2 5 0.76. 1414 1355 1415 1356 1416 1357 1417 1358 provide a clear platform for interpreting evolution- the muscles appear quite slender, and there is no 1418 1359 ary changes in sonic morphology. Howes (1992) neural rocker, rocker bone or winglike process. It 1419 1360 examined the morphology of a large number of is not currently possible to interpret this system 1420 1361 ophidiids, including several aspects of the sonic as primitive or, rather, a degenerate adaptation to 1421 1362 system without considering function. He separated the deep sea. Splitting of the ventral muscles into 1422 1363 the ophidiids into two major patterns: (1) those lateral and medial components would argue that 1423 1364 with direct contacts between the swimbladder and this adaptation is not basal. 1424 1365 expanded ribs, and (2) those in which the swim- The second basic pattern is found in the fawn 1425 1366 bladder is isolated from nonexpanded ribs. Our cusk-eel (this study) and the striped cusk-eel Ophi- 1426 1367 discussion here will concentrate on studies focused dion marginatum (Courtenay, 1971). Although 1427 1368 primarily on the sonic mechanism, which all there are major differences in swimbladder mor- 1428 1369 appear to come from Howe’s first group. These phology, both species have ventral, intermediate, 1429 1370 studies indicate extreme variability, and sonic and dorsal muscles. Courtenay’s ventral muscles 1430 1371 mechanisms examined fall into three patterns. (his primary sonic muscles) connect to the winglike 1431 1372 The simplest system is present in the deep-water process (his bladelike first ribs) in males but to 1432 1373 Barathrodemus manatinus, collected from 1,800– thickened outpocketings of the anterior bladder in 1433 1374 2,600 m (Carter and Musick, 1985). Males possess females. In the fawn cusk-eel, ventral muscles con- 1434 1375 two ventral muscles (a lateral and a medial) that nect to the winglike process and swimbladder in 1435 1376 both originate on the prootic. The lateral muscle, both sexes. Courtenay finds a medial sound-pro- 1436 1377 present only in males, inserts on the swimbladder ducing muscle (5 our intermediate muscle) only in 1437 1378 wall, and the medial muscle inserts broadly on females, whereas it is present in both sexes in the 1438 1379 ribs attached to vertebra 4 in males and females. fawn cusk-eel and enlarged in females. Courtenay 1439 1380 Compared to development in more shallow forms, mentions that the dorsal muscles insert broadly on 1440

Journal of Morphology DOI 10.1002/jmor

ID: vasanss Date: 15/6/07 Time: 15:50 Path: J:/Production/JMOR/Vol00000/070042/3B2/C2JMOR070042 J_ID: JMOR Wiley Ed. Ref. No.: 1697 Customer A_ID: JMOR10551 Date: 15-JUNE-07 Stage: I Page: 13

SONIC MORPHOLOGY IN LEPOPHIDIUM PROFUNDORUM 13 1441 the distal anterior surfaces of the first neural ACKNOWLEDGMENTS 1501 1442 spine (our neural rocker). Our thin dorsomedial 1502 Samples were collected during fishery independ- 1443 muscle that inserts medially on the apex of the 1503 ent bottom trawl surveys and were provided by 1444 neural rocker has not been previously described. 1504 the Ecosystem Surveys Branch of the Northeast 1445 However, Courtenay states that the dorsal muscle 1505 Fisheries Science Center, NOAA Fisheries. Our 1446 is weakly attached to the medial surface of the 1506 thanks to Peter Chase for helping us procure the 1447 spine with connective tissue that is easily torn. 1507 fish and to Michael Fahay for providing some fixed 1448 His observation could reflect the incipient forma- 1508 specimens. 1449 tion or loss of this muscle. Notably, the dorsal 1509 1450 muscle in the striped cusk-eel is so much larger 1510 1451 than the ventral muscle in males that the struc- LITERATURE CITED 1511 1452 ture can be recognized externally as a hump on 1512 Alexander RM. 2002. Tendon elasticity and muscle function. 1453 the head. The fawn cusk-eel is sexually monomor- Comp Biochem Physiol A 133:1001–1011. 1513 1454 phic, and the vental and dorsal muscles are simi- Amorim MCP, Hawkins AD. 2005. Ontogeny of acoustic and 1514 1455 lar in size in males in our spring and fall samples, feeding behaviour in the Grey Gurnard Eutrigla gurnardus. 1515 1456 both of which appear to be outside of the mating Ethology 111:255–269. 1516 1457 season. Bass AH, Baker R. 1991. Evolution of homologous vocal control 1517 traits. Brain Behav Evol 38:240–254. 1458 The third pattern is present in some Ophidion Bass AH, McKibben JR. 2003. Neural mechanisms and behav- 1518 1459 (Ophidiidae) and Onuxodon (Carapidae), which iors for acoustic communication in teleost fish. Prog Neurobiol 1519 1460 have a rocker bone protruding from the front wall 69:1–26. 1520 1461 of the swimbladder (Rose, 1961; Tyler, 1970; Par- Bradbury JW, Vehrencamp SL. 1998. Principles of Animal Com- 1521 munication. Massachusetts: Sinauer. 1462 mentier et al., 2006a). In Ophidion barbatum, suc- Carter HJ, Musick JA. 1985. Sexual dimorphism in the deep- 1522 1463 cessive contractions of the ventral and dorsal sea fish Barathrodemus manatinus (Ophidiidae). Copeia 1523 1464 muscles cause counter clockwise and then clock- 1985:69–73. 1524 1465 wise rotation of the rocker bone, resulting in the Casadevall M, Matallanas J, Carrasson M, Mun˜ oz M. 1996. 1525 1466 inward and outward deformation of the swimblad- Morphometric, meristic and anatomical differences between 1526 Ophidion barbatum L., 1758 and O. rochei Mu¨ ller, 1845 (Pis- 1467 der (Parmentier et al., 2006a). We suggest that the ces, Ophidiidae). Publ Esp Inst Esp Oceanogr 21:45–61. 1527 1468 intermuscular tendon and the anterior wall of the Chao LN. 1978. A basis for classifying Western Atlantic Sciaeni- 1528 1469 swimbladder in the fawn-cusk-eel may be a precur- dae (Teleostei: Perciformes). Washington DC: National Oce- 1529 1470 sor to the rocker bone (see also Parmentier et al., anic and Atmospheric Administration. 1530 Collette BB, Klein-MacPhee G. 2002. Bigelow and Schroeder’s 1471 2002; Parmentier and Diogo, 2006). Fishes of the Gulf of Maine, 3rd ed. Washington: Smithsonian 1531 1472 Measurements of sonic structures in this study Institution.748 p. 1532 1473 provide the first quantitative treatment of sexual Connaughton MA. 2004. Sound generation in the searobin 1533 1474 dimorphism in this family. Larger intermediate (Prionotus carolinus), a fish with alternate sonic muscle con- 1534 1475 muscles in female fawn cusk-eels and their pres- traction. J Exp Biol 207:1643–1654. 1535 Connaughton MA, Taylor MH. 1995. Effects of exogenous tes- 1476 ence in females but not males in striped cusk-eels tosterone on sonic muscle mass in the weakfish, Cynoscion 1536 1477 (Courtenay, 1971) clearly reverses the normal regalis. Gen Comp Endocrinol 100:238–245. 1537 1478 trend in sound production in which a sonic mecha- Connaughton MA, Fine ML, Taylor MH. 2002. Weakfish sonic 1538 1479 nism is either larger or present only in males of muscle: Influence of size, temperature and season. J Exp Biol 1539 205:2183–2188. 1480 many fish species (Ladich and Fine, 2006). Several Courtenay WR. 1971. Sexual dimorphism of the sound produc- 1540 1481 structures in the male (notably dorsal muscle ing mechanism of the striped cusk-eel, Rissola marginata 1541 1482 weight, ventral muscle tendon length, neural (Pisces: Ophidiidae). Copeia 1971:259–268. 1542 1483 rocker weight, winglike process weight, and swim- Courtenay WR, McKittrick FA. 1970. Sound-producing mecha- 1543 1484 bladder weight) grow at a greater rate in males nisms in carapid fishes, with notes on phylogenetic implica- 1544 tions. Mar Biol 7:131–137. 1485 suggesting androgenic control (Fine and Penny- Crawford JD, Huang X. 1999. Communication signals and 1545 1486 packer, 1986; Connaughton and Taylor, 1995; Fine, sound production mechanisms of mormyrid electric fish. J 1546 1487 1997). However, the occurrence of similar slopes Exp Biol 202:1417–1426. 1547 1488 yet significant differences in lengths for all sonic Fine ML. 1978. Seasonal and geographic variation of the mat- 1548 ing call of the oyster toadfish Opsanus tau. Oecologia 36:45– 1489 muscles in males and females is difficult to inter- 57. 1549 1490 pret. The same is true for equivalent regression Fine ML. 1997. Endocrinology of sound production in fishes. 1550 1491 slopes of the ventral and intermediate muscle Mar Freshwater Behav Physiol 29:23–45. 1551 1492 weights between males and females. One possible Fine ML, Pennypacker KR. 1986. Hormonal basis for sexual 1552 1493 cause would be a hormonal effect during a critical dimorphism of the sound producing apparatus of the oyster 1553 toadfish. Exp Neurol 92:289–298. 1494 period coinciding with initial gonad maturation. Fine ML, Malloy KL, King CB, Mitchell SL, Cameron TM. 1554 1495 The greater muscle lengths and weights, extended 2001. Movement and sound generation by the toadfish swim- 1555 1496 tips on the winglike process, and a more massive bladder. J Comp Physiol A 187:371–379. 1556 1497 swimbladder with a more developed fenestra sug- Fine ML, Schrinel J, Cameron TM. 2004. The effect of loading 1557 1498 on disturbance sounds of the Atlantic croaker Micropogonius gest that males are capable of producing more undulatus: Air vs. water. J Acoust Soc Am 116:1271–1275. 1558 1499 intense sounds than females, presuming that Howes GJ. 1992. Notes on the anatomy and classification of 1559 1500 females can call at all. ophidiiform fishes with particular reference to the abyssal 1560

Journal of Morphology DOI 10.1002/jmor

ID: vasanss Date: 15/6/07 Time: 15:50 Path: J:/Production/JMOR/Vol00000/070042/3B2/C2JMOR070042 J_ID: JMOR Wiley Ed. Ref. No.: 1697 Customer A_ID: JMOR10551 Date: 15-JUNE-07 Stage: I Page: 14

14 M.L. FINE ET AL. 1561 genus Acanthonus Gu¨ nther, 1878. Bull Br Mus Nat Hist Perkins PJ. 2001. Drumming and chattering sounds recorded 1621 1562 (Zool) 58:95–131. underwater in Rhode Island. Northeastern Nat 8:359–370. 1622 1563 Ladich F, Fine ML. 2006. Sound-generating mechanisms in Remage-Healey L, Bass AH. 2005. Rapid elevations in both ste- 1623 fishes: A unique diversity in vertebrates. In: Ladich F, Colin roid hormones and vocal signaling during playback challenge: 1564 SP, Moller P, Kapoor BG, editors. Communication in Fishes. A field experiment in Gulf toadfish. Horm Behav 47:297–305. 1624 1565 Enfield, New Hampshire: Science Publishers. pp 3–43. Rome LC, Linstedt SL. 1998. The quest for speed: Muscles built 1625 1566 Mann DA, Jarvis SM. 2004. Potential sound production by a for high-frequency contractions. News Physiol Sci 13:261–268. 1626 1567 deep-sea fish. J Acoust Soc Am 115:2331–2333. Rose JA. 1961. Anatomy and sexual dimorphism of the swim 1627 bladder and vertebral column in Ophidion holbrooki (Pisces: 1568 Mann DA, Bowers-Altman J, Rountree RA. 1997. Sounds pro- 1628 duced by the striped cusk-eel Ophidion marginatum (Ophi- Ophidiidae). Bull Mar Sci 11:280–308. 1569 diidae) during courtship and spawning. Copeia 1997:610–612. Rountree RA, Bowers-Altman J. 2002. Soniferous behaviour of 1629 1570 Marieb EN, Mallatt J. 2001. Human Anatomy, 3rd ed. New the striped cusk-eel Ophidon marginatum. Bioacoustics 12: 1630 1571 York: Benjamin Cummings. 240–242. 1631 Skoglund CR. 1961. Functional analysis of swimbladder Marshall NB. 1967. Sound-producing mechanisms and the biol- 1572 muscles engaged in sound productivity of the toadfish. J Bio- 1632 ogy of deep-sea fishes. In: Tavolga WN, editor. Marine Bio- 1573 phys Biochem Cytol 10:187–200. 1633 Acoustics, Vol. 2. New York: Pergamon. pp 23–133. 1574 Sprague MW. 2000. The single sonic muscle twitch model for 1634 Nielsen JG, Cohen DM, Markle DF, Robins CR. 1999. Ophidii- the sound-production mechanism in the weakfish, Cynoscion 1575 form Fishes of the World (order Ophidiiformes). Rome: FAO. 1635 1576 regalis. J Acoust Soc Am 108:2430–2437. 1636 FAO Species Catalog, Volume 18, 178 p. Sprague MW, Luczkovich JJ. 2001. Do striped cusk-eels. Ophi- 1577 Parmentier E, Diogo M. 2006. Evolutionary trends of swimblad- dium marginatum produce the ‘chatter’ sound attributed to 1637 1578 der sound mechanisms in some teleost fishes. In: Ladich F, weakfish, Cynoscion regalis (Sciaenidae)?. Copeia 2001:854– 1638 1579 Collin SP, Moller P, Kapoor BG, editors. Communication in 859. 1639 Fishes, Vol. 1. Enfield, New Hampshire: Science Publishers. 1580 Tavolga WN. 1964. Sonic characteristics and mechanisms in 1640 pp 45–70. marine fishes. In: Tavolga WN, editor. Marine Bio-Acoustics. 1581 Parmentier E, Chardon M, Vandewalle P. 2002. Preliminary New York: Pergamon. pp 195–211. 1641 1582 study on the ecomorphological signification of the sound-pro- Thorson RF, Fine ML. 2002. Crepuscular changes in emission 1642 1583 ducing complex in Carapidae. In: Aerts P, D’Aouˆ t K, Herrel rate and parameters of the boatwhistle advertisement call of 1643 1584 A, Van Damme R, editors. Topics in Functional and Ecological the gulf toadfish, Opsanus beta. Environ Biol Fish 63:321– 1644 Vertebrate Morphology. Maastrich: Shaker Publishing. pp 1585 331. 1645 139–151. Tyler JC. 1970. A redescription of the inquiline carapid fish 1586 Parmentier E, Fontenelle N, Fine ML, Vanderwalle P, Henrist Onuxodon parvibrachium, with a discussion of the skull 1646 1587 C. 2006a. Functional morphology of the sonic apparatus in structure and the host. Bull Mar Sci 29:148–164. 1647 1588 Ophidion barbatum (Teleostei, Ophidiidae). J Morphol Weston DE. 1967. Sound propagation in the presence of bladder 1648 1589 267:1461–1468. fish. In: Albers VM, ed. Underwater Acoustics, Vol 2. New 1649 Parmentier E, Lagarde`re JP, Braquegnier JB, Vandewalle P, York: Plenum. pp 55–88. 1590 Fine ML. 2006b. Sound production mechanism in carapid Winn HE. 1964. The biological significance of fish sounds. In: 1650 1591 fish: First example with a slow sonic muscle. J Exp Biol Tavolga WN, editor. Marine Bio-Acoustics. New York: Perga- 1651 1592 209:2952–2960. mon. pp 213–231. 1652 1593 1653 1594 1654 1595 1655 1596 1656 1597 1657 1598 1658 1599 1659 1600 1660 1601 1661 1602 1662 1603 1663 1604 1664 1605 1665 1606 1666 1607 1667 1608 1668 1609 1669 1610 1670 1611 1671 1612 1672 1613 1673 1614 1674 1615 1675 1616 1676 1617 1677 1618 1678 1619 1679 1620 1680

Journal of Morphology DOI 10.1002/jmor

ID: vasanss Date: 15/6/07 Time: 15:50 Path: J:/Production/JMOR/Vol00000/070042/3B2/C2JMOR070042