Morphological and Functional Bases of Durophagy in the Queen Triggerfish, Balistes Vetula (Pisces, Tetraodontiformes)

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Morphological and functional bases of durophagy in the Queen Triggerﬁsh, Balistes vetula (Pisces, Tetraodontiformes)

Article in Journal of Morphology · February 1993 DOI: 10.1002/jmor.1052150202

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Ralph G Turingan Peter C Wainwright Florida Institute of Technology University of California, Davis

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Morphological and Functional Bases of Durophagy in the Queen Triggerfish, Balistes vetula (Pisces, Tetraodontiformes)

RALPH G. TURINGAN AND PETER C. WAINWRIGHT Department ofMarine Sciences, llniuersity of Puerto Rico, Mayagiiez, Puerto Rico 00681 (R.G.T.); Department of Biological Science, Florida State University, Tallahassee, Florida 32306-3050 (P.C.W.) ABSTRACT Tetraodontiform fishes are characterized by jaws specialized for powerful biting and a diet dominated by hard-shelled prey. Strong biting by the oral jaws is an unusual feature among teleosts. We present a functional morphological analysis of the feeding mechanism of a representative tetraodontiform, Balistes vetula. As is typical for the order, long, sharp, strong teeth are mounted on the short, robust jaw bones of B. vetula. The neurocranium and suspensorium are enlarged and strengthened to serve as sites of attachment for the greatly hypertrophied adductor mandibulae muscles. Electromyographic recordings made from 11 cranial muscles during feeding revealed four distinct behaviors in the feeding repertoire of B. vetula. Suction is used effectively to capture soft prey and is associated with a motor pattern similar to that reported for many other teleosts. However, when feeding on hard prey, B. vetula directly bit the prey, exhibiting a motor pattern very different from that of suction feeding. During buccal manipulation, repeated cycles of jaw opening and closing (biting) were coupled with rapid movement of the prey in and out of the mouth. Muscle activity during buccal manipulation was similar to that seen during bite-captures. A blowing behavior was periodically employed during prey handling, as prey were forcefully "spit out" from the mouth, either to reposition them or to separate unwanted material from flesh. The motor pattern used during blowing was distinct from similar behaviors described for other fishes, indicating that this behavior may be unique to tetraodontiforms. Thus B.vetula combines primitive behaviors and motor patterns (suction feeding and buccal manipulation) with specialized morphology (strong teeth, robust jaws, and hypertrophied adductor muscles) and a novel behavior (blowing) to exploit armored prey such as sea urchins, molluscs, and crabs, o 1993 Wiley-Liss, Inc.

The biomechanics of prey capture in fishes geal-jaw prey processing have also attracted have been the subject of extensive study by the attention of functional anatomists (Liem, functional morphologists during the past two '78; Lauder, '83b,c; Liem and Sanderson, decades (Liem, '70, '79; Lauder, '80, '83a; '86; Sibbing et al., '86; Sibbing, '88; Wain- Muller and Osse, '84; Muller et al., '82). wright, '89a,b; Sanford and Lauder, '89). Experimental investigations, especially on the Most of these experimental studies have ben- mechanics of upper jaw protrusion, have pre- efitted from the use of sophisticated proce- sented evidence that the design of teleost dures such as electromyography, high-speed feeding systems reflects the common usage of cinematography, cineradiography, and pres- suction feeding (Osse, '69; Liem, '78, '79; sure recordings. These techniques have al- Lauder and Lanyon, '80; Lauder, '80, '83a, lowed the acquisition of an enormous data '85; Lauder and Clark, '84; van Leeuwen, base through which has emerged a solid un- '84; van Leeuwen and Muller, '83, '84; Sib- derstanding of the functional morphology of bing et al., '86; Sanderson, '88; Westneat and Wainwright, '89). However, because prey cap- Address reprint requestdeorrcspondence to Peter C. Wain- ture is only the initial step in feeding behav- wright, Department of Biological Science, Florida State Univer- ior, the mechanisms of intraoral and pharyn- sity, Tallahassee,FI, 32306-3050. o 1993 WILEY-LISS,INC 102 R.G. TURINGAN AND P.C. WAINWRIGHT the musculoskeletal components of the tel- MATERIALS AND METHODS eostean feeding machinery. Specimens and anatomy Two major trends that have been noted Four freshly frozen specimens and five for- during the evolution of feeding systems in malin preserved specimens (95-210 mm stan- teleost fishes are 1) the great majority of dard length; SL) of B. uetula were dissected fishes retain suction feeding, the phylogenet- for osteological and myological analyses. In ically primitive means of prey capture in ver- addition, seven dry skeletons (130-280 mm tebrates, as the principal means of capturing SL; prepared using dermestid beetles) were and ingesting food (Lauder, '83a, '85) and 2) also examined. All specimens examined for associated with this emphasis on suction feed- this study were sexually mature. Freehand ing, many lineages of teleosts possess a highly drawings were made from these specimens mobile and protrusible upper jaw (Schaeffer (Figs. 1, 2). Osteological terminology follows and Rosen, '61; Lauder, '85; Motta, '84). The Matsuura ('79) and Tyler ('go), and myo- majority of teleost species use suction to cap- logical terminology follows Winterbottom ture mobile, unattached animal prey. In rela- (' 74a,b). tively few lineages is this trend reversed. In For electromyographic experiments, four this paper we present an analysis of the feed- live individuals of B. vetula (145-174 mm ing mechanism in the queen triggerfish, Bal- SL) were collected by hand from fringing istes vetula, a representative of a major clade coral reefs off the southwestern coast of of percomorph teleost fishes (the Tetraodon- Puerto Rico. The fish were maintained in tiformes) that exhibits a reversal of both of free-flowing saltwater aquaria at the Marine these trends. Sciences Laboratory of the University of As with most members of the order, B. Puerto Rico for 2 weeks prior to shipment to vetula feeds principally on nonelusive, heavily the Department of Biological Science, Flor- armored prey types that are apparently cap- ida State University. Each fish was main- tured by biting the prey directly (Randall, tained separately in 100 liter aquaria at room '67; Reinthal et al., '84) without the use of temperature (24°C) and fed pieces of squid, suction. Numerous major modifications of live earthworms, live fish, and thawed frozen the cranial skeleton, musculature, and teeth crabs for up to 4 weeks prior to the experi- (including a complete loss of upper jaw protru- ments. These same food types were also used sion) are associated with this durophagous for all feeding experiments. feeding habit and characterize the two lineages of derived tetraodontiforms, the Balis- Electromyography toidei and the Tetraodontoidea (Winterbot- The activity patterns of 11 muscles were tom, '74a). The primary goal of this study is documented using electromyography to exam- to describe the feeding mechanism of a repre- ine the functional role of these muscles dur- sentative tetraodontiform fish and to explore ing feeding in B. vetula. The electromyo- the morphological and functional specializa- graphic procedures followed Wainwright tions for a durophagous feeding habit. We ('89a,b) and Westneat and Wainwright ('89). document the first electromyographic record- Briefly, steel alloy bipolar fine wire (0.002 ings made during feeding in a free-swimming gauge) electrodes were threaded through a tetraodontiform. Functional data on the feed- 26-gauge hypodermic needle. To ensure that ing mechanisms of tetraodontiform fishes are the paired electrode wires did not spread almost completely lacking in the literature apart during the experiment, the first 15 cm (Sarkar, '60; Winterbottom, '74a; Tyler, '80; of wire were glued together using a thin coat Gosline, '87), so a second goal of this paper is of cyanoacrylate adhesive. Approximately 0.5 to lay the foundations for future research on mrn of the plastic coating that insulated the the evolution of the feeding system within wire was scraped off each electrode tip using this diverse clade. Phylogenetic hypotheses a blade under a dissecting microscope. The exist for the major lineages of tetraodon- exposed tips were then bent back against the tiforms (Winterbottom, '74a; Tyler, '80; needle barrel until they were almost parallel Lauder and Liem, '83; Winterbottom and to one another and - 1 mm apart. The bent Tyler, '83; Mok and Shen, '83; Leis, '841,and wire tips also served as hooks that anchored the extensive differences seen among these the electrode into the belly of the muscle taxa in skull anatomy inhcate a potentially during the experiments. rich system for studies of the evolution of the Each experimental fish was anesthetized complex feeding mechanism. using a seawater solution of tricaine methane- FEEDING MECHANISM OF BALISTE'S VETIJLA 103 sulfonate (MS-222; 1.0 g/liter) for - 10 min muscles were simultaneously amplified 10,000 and then transferred to a shallow dissecting times using Grass P511J preamplifiers. A tray containing 50% fresh seawater and 50% bandpass of 100-3,000 Hz was used, and the anesthetizing solution, Up to 10 color coded 60 Hz notch filter was always employed. Ana- electrodes were used during each experi- log recording of electrical signals from the ment, and each electrode was implanted di- muscles were recorded on a Teac XR-5000 rectly into the belly of the target muscle, The tape recorder at a tape speed of 19 cm/sec. electrode wires were glued together to form a The electromyographic recordings were later single cable that was secured to a suture played back at one-fourth the recording speed looped through the skin posterior to the fish's and printed using a Western Graphtec head just lateral to the first dorsal spine. Mark-11 thermal array recorder. All experi- Muscle activity was recorded from the left ments were conducted at room temperature members of the levator operculi (LOP), dila- (24°C * 0.5"C). tor operculi (DO), epaxialis (EP), obliquus To summarize the temporal pattern of mus- inferioris (OBI), sternohyoideus (SH), pro- cle activities, a total of 21 variables (11 dura- tractor hyoidei (PHI (=geniohyoideus), re- tion of activity variables and 10 relative onset tractor arcus palatini (RAP), and four sec- of activity variables) were measured from the tions of the adductor mandibulae muscle (Alol, electromyograms. Average values (with stan- Aza, AzP, Azy) (see Figs. 1 and 2). These dard errors; S.E.) for each EMG duration and muscles were chosen because they have been onset variable were calculated. The duration shown to play major roles in moving the of activity of each of the 11 muscles (see cranial elements of other teleosts during feed- above) was measured directly from the chart ing or because they were anticipated to be of recordings for each feeding (e.g., LOP-DUR). particular interest regarding B. uetula. The To examine the sequence of firing of each symmetrical and asymmetrical firing of mor- muscle, the onset of activity of th levator phologically symmetrical cranial muscles dur- operculi (LOP) was designated as time zero, ing feeding in fishes may be a possible source and, from this point, the relative onset of activity of each of the other 10 muscles was of motor pattern variation (Liem, '79; Lauder determined (e.g., LOP-RAP). The LOP was and Norton, '80). Because simultaneous bilat- chosen as the reference muscle because it eral recordings of the cranial muscles of B. was consistently active in all cycles of muscle uetula were not conducted in this study, the activity and to facilitate comparisons with contribution of this source of variation to the other studies that have used this muscle as a modulation of the oral jaw mechanism in this reference (Wainwright and Lauder, '86;West- fish could not be determined. neat and Wainwright, '89). All measure- To ensure that the electrodes were prop- ments were made manually using a digital erly implanted into the target muscles, sev- caliper (Mitutuyo Series 500) and are ex- eral trial electrode implantations were made pressed in milliseconds. on formalin preserved and thawed, frozen Only some of the 11 muscles were active specimens of B. vetula prior to the actual during each cycle of motor activity for each of electromyographic recordings. We also relied the four feeding behaviors observed (see be- on the relative positions of specific skeletal low). Thus the frequency of activation of landmarks to guide electrode placement. Af- each muscle was calculated as a percentage of ter each electromyographic recording ses- the maximum number of cycles analyzed for sion, the fish was sacrificed using an over- the behavior. An overall frequency of activity dose of the anesthetizing solution and then was computed by averaging the values across dissected to confirm electrode placement. We all four fish. found no electrode that was improperly posi- tioned. RESULTS After implanting the electrodes, experimen- Anatomy of the feeding apparatus tal fish were returned to their aquarium, Osteology where, upon recovery from anesthesia, they In the anatomical descriptions of the queen were offered a variety of prey: 3-5-cm pieces triggerfish that follow, emphasis is given to of squid mantle, 6-10-cm-long live earth- areas of the head that are of particular func- worms (Lumbricus), 3-5-cm (SL) live fish tional interest. Additional osteological and (Poecelza latipinnu), and 1-2 cm (carapace myological descriptions of this species and diameter) fresh/thawed majid crabs (Mzthrax other tetraodontiform fishes are found in sculptus). Electrical signals from up to eight Gregory ('33), Sarkar ('601, Tyler ('68, ,801, 104 R.G. TURINGAN AND P.C. WAINWRIGHT Matsuura ('79), and Winterbottom ('74a). 2A; MX), allowing these bones to function as The musculoskeletal linkages that play signif- a single unit on each side of the upper jaw. icant roles in the feeding repertoire of B. The primary articulation of the upper jaw to uetula include the oral jaws (upper and lower the neurocranium is through a strong liga- jaws), the neurocranium, the suspensorial mentous joint between the concave pos- apparatus, the hyoid apparatus, the opercu- terodorsal edge of the premaxilla and the lar apparatus, and the pectoral girdle (Fig. 1). anterior tips of the ethmoid and the vomer. The neurocranium of B. vetula is elon- The dorsal edge of the maxilla and the dorso- gated rostrocaudally and serves as the dorsal lateral edge of the premaxilla are connected mechanical element of the feeding apparatus to the anterior and anteroventral portions of (Figs. 1, 2). The anterior portion of the skull the palatine. The short and thick lower jaw is dominated by an elongated ethmoid (Fig. consists of the dentaries (Fig. 2A, DN), the 2A; EM) that interdigitates laterally with the articulars (Fig. 2A; AR), and the angulars prefrontals (Fig. 2A; PF) and dorsally with (Fig. 2A; AN). These bones are articulated to the frontals (Fig. 2A; FR). The other skull each other by interdigitation. Each articular bones include the laterally flattened parasphe- is concave posterolaterally to accommodate noid (Fig. 2A; PA) that runs ventral to the the thickened knob of the anterior tip of the ethmoid and the orbit, the relatively small quadrate. Each angular is ventrolaterally con- vomer (Fig. 2A; VO), the sphenotic (Fig. 2A; cave to serve as a joint between the lower jaw SN), and the pterotic (Fig. 2A; PT). The and the interopercular bone (Fig. 2A; 10). anterior region of the neurocranium, particu- Each premaxilla and dentary support an outer larly the anteroventral tip of the ethmoid and row of four long, stout teeth that are notched the vomer, provides points of articulation at their edges and are held closely to one with the upper jaw and the anterodorsal leg another. of the suspensorium. Just below its orbital The greatly reduced opercular apparatus region, the neurocranium articulates via the of B. uetula is modified from the condition pterotic and the sphenotic with the pos- seen in most teleosts. The hyomandibula has terodorsal leg of the suspensory apparatus, an expanded and thickened posterodorsal arm the pectoral girdle, and the opercular series. that articulates with the opercular bone. The The suspensorium is divided into two ma- small, flattened, and leaf-like opercular bone jor regions. The anterior end of the T-shaped palatines (Fig. 2A; PL) represents the an- (Fig. 2A; OP) firmly articulates with the dor- terodorsal leg of the roughly U-shaped sus- sal aspect of the thin subopercular bone (Fig. pensory apparatus. The palatines articulate, 2A; SO) by way of a ligamentous connective anteriorly, through a ligamentous connective tissue. An obvious modification of the opercu- tissue with the ethmoid, vomer, premaxilla lar apparatus is that the interopercular bone (Fig. 2A; PM) and the maxilla (Fig. 2A; MX) (Fig. 2A; 10) has been reduced into a tiny and, posteriorly, with the ectopterygoid (Fig. bony rod. A tough ligament connects the 2A; ET). The ectopterygoid, the mesoptery- anterior tip of this tiny rod shaped bone to goid (Fig. 2A; MS), the metapterygoid (Fig, the ventrolateral concavity in the angular. 24MT), the quadrate (Fig. 2A; QD), and the Posteriorly, the I0has two ligamentous artic- symplectic (Fig. 2A; SM) interdigitate either ulations: One ligament connects it to the completely or slightly with one another. The dorsal aspect of the epihyal, and the other posterodorsal leg of the suspensorium is dom- ligament (Figs. lA, 2B, 2D; IOL) extends inated by the dorsoventrally elongated hyo- posterodorsally to connect this bone to the mandibular bone (Fig. 2A, HM) that articu- ventromedial edge of the opercular bone. This lates primarily with the pterotic and the arrangement represents a retention of the sphenotic. The broad preoperculum (Fig. 2A, phylogenetically primitive mechanical cou- PO) articulates anteriorly with the quadrate pling between this bone and the hyoid bar on and symplectic and posteriorly with the hyo- one hand and the opercular series on the mandibula. Both anterodorsal and pos- other. This arrangement permits depression terodorsal joints between the suspensory ap- of the lower jaw in two ways: 1) by the paratus and the neurocranium (Figs. 1, 2A) depression of the hyoid bar (see below) and 2) allow for slight mediolateral swinging of the by the posterior rotation of the operculo- suspensorium relative to the skull. subopercular bone complex on its articula- Structural deviations from the generalized tion with the hyomandibula. percomorph design are particularly evident The hypohyal (Fig. 2A; HH), the urohyal in the upper and lower jaws. One novel fea- (Fig. 2A; UH), the ceratohyal (Fig. 2A; CH), ture is the almost complete fusion of the the epihyal (Fig. 2A, EH), and the interhyal premaxilla (Fig. 2A; PM) to the maxilla (Fig. (Fig. 2A; IH) are articulated with one an- FEEDING MECHANISM OF BALISTES VETULA 105

OPERCULAR

NEUROCRA NIUM

OPERCULAR SERIES

PECTORAL GIRDLE SUSPENSORI HYOID ARCH

LOWER JAW UPPER JAW C. Fig. 1. Balistes uetula. Schematic diagram of the skull tor mandibulae muscles are not illustrated in order to illustrating the major functional units of the feeding show the position of the retractor arcus palatini. Contrac- mechanism in lateral (A),dorsal (B), and ventral (C) tion of this muscle possibly generates the force that views. Thick lines indicate the attachments of major produces mediolateral movement of the suspensorium. muscles of the feeding mechanism discussed in this pa- Abbreviations as in Figure 2. per. In the dorsal view diagram (B),the superficial adduc- 106 R.G. TURINGAN AND P.C. WAINWRIGHT

C. SH

Fig. 2. Balistes uetula. A: Detailed drawing of the the interopercle, and the sternohyoideus muscle. AN, bones comprising the functional units diagrammed in angular; AR, articular; Ala, Aza, AzP, APysections of the Figure 1. Note the reduced size of the opercular series adductor mandibulae; CC, coracoid; CH, ceratohyal; CT, bones and the expanded rostra1 region of the neurocra- cleithrum; DN, dentary; DO, dilator operculi; EH, epi- nium and the suspensorium that serve as sites of attach- hyal; EP, epaxialis; EM, ethmoid; ET, ectopterygoid; FR, ment for the adductor mandibulae muscles. B: Lateral frontal; HH, hypohyal; HM, hyomandibula; IH, inter- view diagram of the superficial muscles of the head. Note hyal; 10, interopercle; IOL, interopercle-opercle liga- the distinct sections of the adductor mandibulae com- ment; LOP, levator operculi; MS, mesopterygoid; MT, plex. C : Deeper view of the adductor mandibulae mus- metapterygoid; MX, maxilla; OBI, obliquus inferioris; cles. The musculoskeletal components of the suspenso- OP, opercle; PA, parasphenoid; PF, prefrontal; PH, rium, hyoid apparatus, opercular series, and the pectoral protractor hyoidei; PL, palatine; PM, premaxilla; PO, girdle were removed to expose the deeper structures. D: preopercle; PT, pterotic; QD, quadrate; RAP, retractor An even deeper dissection of the palatal region is illus- arcus palatini; SC, supracleithrum; SH, sternohyoideus; trated to show the position of the retractor arcus palatini. SM, symplectic; SN, sphenotic; SO, subopercle; UH, Also illustrated is the opercular coupling to the jaw via urohyal; VO, vomer. other by way of cartilagenous and ligamen- The pectoral apparatus is notably enlarged. tous tissues or through interdigitation to form It is dominated by the coracoid (Fig. 2A; CC) the hyoid apparatus of B. uetula. The hyoid and the cleithrum (Fig. 2A; CT). These are bar is linked to the suspensorium by way of a broad, elongate bones, attached by fibrous ligamentous joint between the interhyal and connective tissue. The major contribution of the symplectic. Movement of the hyoid appa- the pectoral girdle to the feeding machinery ratus is translated to the lower jaw or to the of B. vetula appears to be its role as a site of opercular bones via the interopercular bone, attachment for important muscles such as which is ligamentously articulated to the epi- the sternohyoideus and the obliquus inferi- hyal. oris. FEEDING MECHANISM OF BALZSTES VETULA 107 Myology The levator operculi (Fig. 2B; LOP) is a The adductor mandibulae muscle complex small muscle originating from the pterotic is enlarged and subdivided in B. vetula (and and supracleithrum and inserting on the pos- in other tetraodontiforms) relative to the phy- terodorsal surface of the opercular bone. The logenetically primitive condition. There are fibers of the dilator operculi (Fig. 2B; DO) six subdivisions of the almost completely par- originate from the sphenotic and insert on allel-fibered adductor mandibulae muscle of the dorsolateral surface of the opercular bone. B. vetula (Winterbottom, '74a): Ala, Alp, The posterodorsal force of the LOP primarily Aza, A$, Azy, and AS. Both A$ and AS are causes the opercular bone to rotate pos- very small and completely covered by the terodorsally about its articulation to the hyo- other subdivisions of the adductor mandibu- mandibula. Contraction of the DO is pre- lae. Except for the small anterior portion dicted to produce a similar action. that is superficially visible in lateral view, The fibers of the protractor hyoidei (Fig. Ala is overlain by Aza (Fig. 2B). The latero- 2B; PHI originate from the skin, the branchio- ventral edges of the ethmoid and prefrontals, stegal rays, and the hypohyal and insert on the infraorbital ligament, and the anterodor- the ventral edge of the lower jaw. The super- sal surface of the hyomandibula serve as sites ficial posterolateral fibers of the sternohyoi- of origin for the fibers of Ala, which insert by deus (Fig. 2B; SH) run continuously with the a tendon mainly on the ventromedial edge of obliquus inferioris (Fig. 2B; OBI). The more the maxilla (Fig. 2C). Contraction of the Al interior portion of the SH (Fig. 2D) is small sections of the adductor mandibulae would relative to the condition seen in most tel- be expected to cause the upper jaw to rotate eosts. This interior section originates from posterodorsally around its point of articula- the anterodorsal edge of the cleithrum, with tion with the neurocranium. The fibers of some of the fibers forming a small bundle AZa originate from the lateroventral portions that originates from the anterior tip of the of the ethmoid, the prefrontals, the infraor- cleithrum and insert on the posterior tip of bital ligament, and portions of the lateral the urohyal (Fig. 2D; SH). The entire SH surface of the hyomandibula. Section A2P inserts on the urohyal with some fibers insert- originates from portions of the hyomandibu- ing on the hypohyal. Contraction of the SH lar, preopercular, and metapterygoid bones. muscle fibers depresses the hyoid bar in gen- The smallest of the A2 subsections, A,y, orig- eralized teleosts, and, although this muscle inates mostly from the lateral surfaces of the and the hyoid bar are both reduced in B. ventral arm of the preopercular bone ventral vetula, the same function is expected for this to the prominent ridge that separates this species. Additional force to depress the hyoid muscle from the adductors dorsally. All three apparatus is apparently generated by the pos- sections of A2 converge anteriorly to insert by terior rotation of the pectoral girdle produced a common tendon on the posterodorsomedial by the contraction of the OBI muscle fibers. edge of the dentary (Fig. 2B). When these As in other teleosts, the epaxialis (Fig. 2B; muscles contract, they pull directly on the EP) is the dominant component of the dorsal dentary, presumably causing the lower jaw to one-half of the Iateral body musculature in B. rotate posterodorsally around the joint be- uetula (Osse, '69; Liem, '70, '78, '79; Lauder, tween the articular and the quadrate. Be- '80, '83b,c; Lauder and Clark, '84; Lauder cause some fibers of Aza and A2P insert on and Liem, '83; Sibbing et al., '86). the tendon that connects the maxilla to the dentary, contraction of these muscles may Patterns of muscle activity also cause slight movement of the upper jaw. Recordings of motor activity were made The retractor arcus palatini (Fig. 2; RAP) during four distinct feeding behaviors: 1)cap- is massive in B. vetula. The fibers of the RAP ture of soft and elusive prey, 2) capture of run parallel to one another and originate hard prey, 3) buccal manipulation, and 4) primarily from the lateral faces of the eth- blowing (or "spitting out") (Figs. 3-8). Here moid and parasphenoid. The muscle is subdi- we describe the basic motor patterns that vided by a tendon that runs posterodorsally were observed during these behaviors. In spite between the ectopterygoid and the prefrontal of the morphological specializations related (Fig. 2D). The RAP inserts on the anterodor- to durophagy, B. vetula usually employed sal surfaces of the bones that compose the suction feeding to capture elusive (fish) and anterodorsal leg of the suspensory apparatus soft (earthworm and pieces of squid) prey (see Results, Osteology). items during our experiments. However, 108 R.G. TURINGAN AND P.C. WAINWRIGHT

500 msec RAP , I '1

I II w Ic----u 3 ru 0 p: U w4 3 c B U C CA L MA NIP U L ATION Q Q T 0

Fig, 3. Balistes uetula. Simultaneous electromyo- triturated. This sequence concluded with a single blow- graphic recordings from five cranial muscles during feeding event as the fish discarded unwanted material imme- ing on a live fish. This sequence illustrates the sequence diately before swallowing the prey. Vertical scale bar at of behaviors typical of feeding on soft and elusive prey. the end of each EMG represents 100 microvolts. Abbrevi- Prey capture is followed by > 20 cycles of buccal manipu- ations as in Figure 2. lation, during which the prey is repeatedly bitten and when feeding on crab a different behavior muscles examined (Figs. 3,4, 7A). The activ- was elicited. ity periods of all muscles overlapped exten- The motor pattern observed during suction- sively. The cycle of muscular activity during type prey capture was characterized by a this phase of the feeding repertoire of B. single, short burst of activity in all of the uetula lasted for an average of 150.69 msec FEEDING MECHANISM OF BALISTES VETULA 109 tion feeding sequences even involving the most mobile fish prey (Fig. 8). In contrast, all LOP four adductor mandibulae muscles showed a 1long, high-amplitude burst of activity in 100% of the suction-type prey capture sequences analyzed (Figs. 7A, 8).Activity in the Ala and Aza muscles began -30 msec following the onset of LOP activity, followed by A2P and A27 which began firing around 40 msec after the onset of LOP activity (Fig. 7A). The motor pattern associated with the capture of crabs was qualitatively different from that observed during suction feeding. B. uetula did not usually appear to employ suction feeding when capturing crab prey but instead directly bit the prey, usually removing an appendage or a piece of the carapace. This behavior was characterized by nonoverlap- ping activity of the mouth opening muscles (i.e., LOP and DO) and the other nine mus- 100 msec cles (Fig. 7B). Activities in the jaw closing muscles (i.e., adductor mandibulae) did not begin until - 90 msec after the onset of LOP PH activity. Only the Ala, A&, and LOP were consistently active during all crab prey capture events (Fig. 8). Very short activities were typical of the epaxialis and obliquus inferioris muscles. The cycle of muscular activity during this phase of the feeding repertoire of B. vetula lasted for an average of 313.40 msec (221.14S.E., N = 47). Processing began immediately after prey were captured and held between the teeth of the upper and lower jaws. Reduction of large prey occurred by repeated sequences of biting I the food between the oral jaws, coupled with rapid movements of the prey in and out of the Fig. 4. Buliskes uetula. Simultaneous electromyographic recordings from five cranial muscles during suc- mouth. We follow Lauder (’83a) in terming tion feeding on a fish prey. Note that this behavior is this behavior as “buccal manipulation.” In characterized by overlapping activity in all muscles. Ver- B. uetula, buccal manipulation involved a tical scale bar at the end of each EMG represents 100 continuous series of up to 23 cycles of alter- microvolts.Abbreviations as in Figure 2. nating activity in the major mouth opening muscles (i.e., LOP and DO) and the major (521.14 S.E., N = 14). The retractor arcus mouth closing muscles (i.e., adductor mandib- palatini was active in all suction-type prey ulae sections Ala, A&, AzP, and A271 (Figs. 3, capture cycles examined (Fig. 8) and was the 5). Each cycle of muscular activity (Fig. 7C) only muscle to show activity prior to the lasted for an average of 215.65 msec (28.73 onset of the levator operculi (LOP) activity S.E., N = 113) and was characterized by short (Fig. 7A). The LOP and dilator operculi (DO) bursts of activity in the LOP and DO muscles began activity simultaneously, and the DO ( - 50 msec), followed by longer bursts in the continued contraction for slightly longer than jaw adductors (>100 msec), and low level the LOP (Fig. 7A). Activity in the other mus- activity in the lateral body musculature (i.e., cles began -20 msec following the onset of epaxialis [EP] and obliquus inferioris [OBI]). LOP activity. The sternohyoideus and pro- The four adductor mandibulae muscles were tractor hyoidei muscles exhibited the most active in virtually all buccal manipulation infrequent and variable activities during suc- cycles, while the sternohyoideus, protractor 110 R.G. TURINGAN AND P.C. WAINWRIGHT I DO&- c .+-+ -', .

P U nu W Cycle 1 Cycle 2 Cycle 3

- 100 msec

Fig. 5. Balistes vetula. Simultaneous electromyo- overlapping, their activity occurs between burst of activ- graphic recordings of four cranial muscles showing three ity of the dilator operculi. Vertical scale bar at the end of cycles of muscular activity during buccal manipulation of each EMG represents 100 microvolts. Abbreviations as in a crab prey. Note that, while the adductor mandibulae Figure 2. and retractor arcus palatini muscles are almost entirely hyoidei, EP, and OBI were infrequently ac- to exhibit long activity bursts during both tive (Fig. 8). prey capture and buccal manipulation (e.g., The blowing behavior occurred under two adductor mandibulae and retractor arcus types of circumstances. In the first type, blow- palatini muscles) exhibited shorter, less regu- ing was used to manipulate prey before cap- lar bursts of activity during blowing (Fig. 7). ture, while, in the second and more common The cycles of muscular activity during this type, blowing was used after prey capture phase of the feeding process lasted for an during the prey manipulation phase to force- average of 219.4 msec (k49.6 S.E., N = 18). fully expel the prey from the mouth. This activity often was preceded and followed by DISCUSSION bouts of buccal manipulation. The diet of B. vetula is dominated by hard- The motor pattern during blowing was shelled and spiny benthic invertebrates such characterized by a very long burst of activity as sea urchins, decapod crabs, pelecypods, in the LOP (Figs. 6, 7D). This prolonged gastropods, and chitons (Randall, '67; Fricke, burst of activity of the LOP was accompanied '71, '75; Reinthal et al., '84). This diet is by extended mouth opening observed while typical of both tropical and temperate mem- the fish exhibited the blowing behavior. Most bers of the genus as well as of other balistids of the other muscles fired toward the end of (Hiatt and Strasburg, '60; Randall, '67; the activity period of the LOP, except for the Fricke, '71, '75; Hobson, '74; Frazer et al., DO, which fired at the same time as the LOP, '91). Armored prey are not normally quick or and the epaxialis, which fired a little later otherwise elusive but require extensive han- (Fig. 7D). Several of the muscles that tended dling and manipulation to break apart the FEEDING MECHANISM OF BALISTES VETIJLA 111

I DO

OBI 100 msec

Fig. 6. Balistes uetula. Simultaneous electromyo- for long periods while material is expelled from the graphic recordings of five cranial inuscles made during a mouth by water currents. Vertical scale bar at the end of single blowing behavior. This behavior is dominated by each EMG represents 100 microvolts.Abbreviations as in activity in the levator operculi muscle, which is activated Figure 2. protective coverings. This study has identi- Structural design of the feeding apparatus fied several morphological and functional (motor pattern) specializations of the feeding The head of B. vetula shows a mixture of mechanism in B. vetula that diverge fromthe derived and primitive features related to the more generalized percomorph feeding condi- durophagous habit of the species. Both the tion and, in conjunction with numerous re- upper and lower jaw bones are equipped with tained primitive features, are employed dur- very strong teeth that are tightly arranged ing prey capture and handling of diverse prey together and have notched edges (Fig. 2). types. Key specializations related to duroph- Fusion of the premaxilla with the maxilla agy include 1) complete loss of jaw protrusion accompanied by loss of upper jaw protrusion and the development of a firm connection provides a jaw system that is braced firmly between the neurocranium and the fused against the neurocranium for support when upper jaw bones; 2) hypertrophy of the adduc- the adductor mandibulae muscles close the tor mandibulae muscles and their sites of mouth (Barel, '83; Otten, '83). Both the lower attachment; 3) presence of stout, anteriorly and upper jaws are shortened, such that the oriented teeth; 4) ability to capture prey ei- outlevers resisting the adductor mandibulae ther by using suction or by biting and pres- muscles (i.e., the distance from the site of ence of distinct motor patterns €or these two rotation of each jaw and the toothed surface) behaviors; and 5) extensive use of blowing are extremely small relative to the size of the during prey handling and a novel motor pat- fish. This arrangement tends to maximize tern associated with this behavior. Below we the resultant force experienced at the contact discuss these, and other specializations re- point between the teeth and prey. lated to the durophagous feeding habits of B. The musculature of the skull is dominated vetula. by the adductor mandibulae complex, which 112 R.G. TURINGAN AND P.C. WAINWRIGHT LOP I LOP DO A. DO A, a - A, a A& A2a A,B A2P AZY A27 RAP RAP PH PH SH SH OBI OBI EP EP

I i~ I I I -25 20 65 110 155 200 -25 20 65 110 155 200 TIME (msec) TIME (msec)

LOP DO A, a A2a Ad A2Y RAP PH PH c SH SH OBI OBI j -* EP EP j N = 4-18

-25 20 65 110 155 200 -25 20 65 110 155 200 TIME (msec) TIME (rnsec)

Fig. 7. Balietes uetula. Bar diagrams summarizing difference in muscle activity patterns between suction the temporal pattern of muscle activity in 11 cranial feeding (A) and biting (B)types of prey capture. Biting muscles during capture of live earthworm and pieces of involves less overlap of activity between the mouth squid prey by suction feeding (A), capture of crab prey by opening muscles (LOP and DO) and the mouth closing biting (B),buccal manipulation of crab prey (C),and muscles (adductor mandibulae) than is seen during suc- blowing of crab prey (D).The length of each bar indicates tion feeding. Capture by biting is very similar to the the mean duration of activity of each muscle, with the motor pattern seen during buccal manipulation (C). The S.E.of duration indicated at the right end of each bar and motor pattern exhibited during blowing (D) is qualita- the S.E. of the onset time indicated at the left end of each tively different from that reported to occur in other fish bar. These bar diagrams summarize data collected from taxa during similar behaviors. Abbreviations as in Figure four individual fish. The range of the sample sizes (N) for 2. each muscle analyzed for each behavior is given. Note the is both hypertrophied and subdivided rela- apparently influenced the construction of the tive to more generalized fishes. Two subdivi- bony elements of the feeding apparatus. sions insert on the upper jaw (Ala and Alp), There is an elongate ethmoid region of the and four subdivisions insert on the lower jaw skull, a ventral expansion of the parasphe- (AZCU,At@, A2y, and &). The modifications of noid, a laterally concave shape of the ptery- the adductor mandibulae and the distribu- goid bones (especially the metapterygoid), a tion of the other muscles of the head have broad preoperculum, and an enlargement of FEEDING MECHANISM OF BALISTES VETULA 113

100 - z 2+ 80 - u 3 60 - u) W 40 - IE 3 I- n 20 - d 0 0 -

lOQ - T 9.2

80 - W 4 m 60 - UI LT 40 - J I- LL 20 - 4 0 0 m -

loor 4.5

P rns

100 - z 21.8 0 I- 80 -

- axznm gqT$~mmnuo

Fig. 8. Balistes uetula. Summary diagram showing average number of cycles for each behavior is given. Note the frequency of activation of each muscle expressed as a that the levator operculi (LOP) was consistently active percentage of the maximum number of cycles exhibited (i.e., 100% activation) during all cycles of muscle activi- during each behavior in the feeding repertoire. Each bar ties analyzed for each behavior, so its bar is not included of the graph shows the average value for all four fish. in each graph. Abbreviations as in Figure 2. Error bars represent standard error of the mean. The 114 R.G. TURINGAN AND P.C. WAINWRIGHT the hyomandibula (Fig. 2A). These enlarged ingly, all of these behaviors have been re- structures serve as sites of attachment for ported in other fish taxa, although their phy- the adductor mandibulae sections. The rigid- logenetic distribution is not clear in every ity and the structural strength of the bony case. Here we contrast these behaviors and elements are apparently enhanced by the the motor patterns associated with them, tough ligamentous and sutural joints be- and discuss the relative evolutionary novelty tween them, such as those connecting the of each. bones of the suspensorium, oral jaws, neuro- In spite of the apparent reduction in em- cranium, and hyoid apparatus. phasis on suction feeding in B. uetula, this The sternohyoideus is reduced in size, as is species retains the ability to capture soft and the hyoid apparatus. It has a novel medial elusive prey (e.g., pieces of squid, live earth- subdivision that runs dorsally to attach the worm, and live fish) using strong suction. tip of the cleithrum to the posterior tip of the The motor pattern exhibited during capture urohyal, rather than to its keel. of prey by suction in B. vetula, which is Another important modification in the feed- characterized by overlapping activity in all of ing apparatus of B. uetula is the presence of the muscles recorded, is similar to the motor the retractor arcus palatini (RAP) muscle, pattern exhibited during suction feeding by which apparently develops as an anterior other percomorph teleosts (Liem, '78, '79; subdivision of the levator arcus palatini (Win- Lauder, '83b; Westneat and Wainwright, '89). terbottom, '74a). Among the Tetraodonti- When the force generated by the firing of the formes, the RAP is present only in the Balis- sternohyoideus and obliquus inferioris mus- toidei land apparently convergently in the cles is unopposed by any activity in the pro- Acanthuridae (Winterbottom, '74a)l. This tractor hyoidei, a posteroventral movement large, parallel-fibered muscle runs anteroven- of the hyoid apparatus probably occurs. This trally from the lateral surface of the ethmoid and the parasphenoid to insert on the pala- downward movement not only lowers the tine and the ectopterygoid (Fig. 2D). It re- floor of the buccal cavity but also enhances places the levator arcus palatini as the prime the opening of the mouth by further depres- adductor of the palatal arch. In most teleosts, sion of the lower jaw. lateral movement of the palatal arch is pro- A particularly interesting feature of the duced by the contraction of the levator arcus motor pattern exhibited by B. uetula at the palatini (Osse, '69;Liem, '70, '78, '79; Lauder, beginning of the suction feeding cycle (Fig. '79, '83b; Lauder and Lanyon, '80). 7A) is the firing of the RAP - 5 msec prior to Among the retained primitive characteris- jaw opening and continuing well beyond the tics of B. vetula (and other tetraodontiforms), initiation of upper and lower jaw adduction the most striking is the presence of a very (i.e., closing of the mouth). This was the only small, undeveloped pharyngeal jaw appara- muscle examined that was active during the tus (Tyler, '80;Winterbottom, '74a). Many of initial stages of the strike, with the levator the other groups of percomorph fishes that operculi and dilator operculi. This unusual have diets of primarily hard-shelled prey have pattern is similar to the activity of the levator greatly hypertrophied pharyngeal jaw bones, arcus palatini during suction feeding in other teeth, and muscles (e.g., Liem and Green- teleosts (Lauder, '79, '81; Liem, '70, '78, '79; wood, '81; Wainwright, '87, '88). It is clear Lauder and Lanyon, 'SO). In spite of the that B. uetula is able to handle armored prey novelty of the separate RAP, these two mus- without the aid of a powerful crushing appa- cles appear to function in much the same ratus in the pharyngeal jaws and that virtu- fashion during suction feeding. Contraction ally all of the functions involved in capture of the RAP in B. uetula applies a posterodor- and reduction of prey are accomplished by sal force on the palatal arch, causing it to the oral jaws. rotate outward. This slight lateral movement of the suspensory apparatus has two possible Motorpatterns and feeding behavior functions: 1) it contributes to early expan- The queen triggerfish appears to rely on a sion of the buccal cavity, thus reducing the combination of four distinct behaviors to cap- pressure inside the oral cavity, or 2) it stabi- ture and process a broad range of prey types: lizes the joint between the palatal arch and 1)inertial suction to capture soft and elusive the neurocranium. In B. vetula, the latter prey, 2) direct biting to capture hard shelled may be important in conjunction with the prey or those attached to the substrate, 3) action of the adductor muscles during buccal buccal manipulation, and 4)blowing. Interest- manipulation (see below), particularly those FEEDING MECHANISM OF BALZSTES VETULA 115 adductor mandibulae sections that arise patterns exhibited during suction feeding and partly from the neurocranium. blowing. At least two features clearly distin- Another noteworthy feature of the suction guish this motor pattern from that seen dur- feeding motor pattern was the low level activ- ing suction feeding: 1) activities of the leva- ity in the epaxialis (EP). Strong activity of tor operculi (LOP) and the dilator operculi EP is associated with the strike in other (DO) do not overlap with activity in any other teleosts ie.g., Liem, '79, '80; Wainwright and muscles and 2) retractor arcus palatini (RAP) Lauder, '86; Wainwright et al., '89) as part of activity does not commence until -30-40 the mechanism involved in elevating the cra- msec following the offset of the LOP and DO. nium. Kinematic analysis of suction feeding During buccal manipulation, the jaws are in B. vetula will be necessary to determine if opened and closed cyclically as the prey is cranial elevation is a significant component moved in and out of the dentigerous area by of cranial movements during the strike. Be- water motion. The repetitious cycle of muscle cause of the low level of activity in the EP, activity involving mouth opening (caused by cranial elevation may not be significant dur- the short burst of activity of the LOP and ing the strike. DO) followed by the prolonged bursts of activ- Activity of the mouth closing muscles over- ities of the addudor mandibulae muscles (i.e., laps substantially with activity in many of Ala, Aza, A2P, Azy) apparently functions to the muscles that apparently expand the reduce the prey, ultimately into smaller pieces mouth cavity (Fig. 7A). This feature is also that can be swallowed. Activity in the RAP typical of other percomorphs (Lauder, '85). during the jaw adduction phase may stabilize The contraction of the upper and lower jaw the suspensorium anteriorly, providing a adductors immediately after mouth opening more solid framework against which the A1a, results in a biting action as both jaws move A2a, A$, and A2y may act. The almost simul- against each other to forcefully grasp the taneous firing of the protractor hyoidei, ster- prey between the teeth. The antagonistic ac- nohyoideus, and obliquus inferioris muscles tion of the protractor hyoidei (contraction of following adduction of the oral jaws may this muscle apparently pulls the hyoid appa- contribute to the stabilization of the floor of ratus anterodorsally, thus elevating the floor the buccal cavity as the jaws close forcefully of the buccal cavity) and the combined forces against the prey. Activity of the ventral mus- of the sternohyoideus and obliquus inferioris culature may also aid in creating a water flow (contraction of these muscles pulls on the that moves the prey posteriorly during mouth hyoid apparatus posteroventrally) after the closing. mouth is fully closed apparently stabilizes Although this behavior appears to conform the hyoid bar in preparation for buccal manip- to "buccal manipulation" as defined by ulation of prey. Lauder ('83a), there are few comparative data Prey capture by biting has been studied for oral jaw muscles during buccal manipula- electromyographically only in some cichlid tion in other percomorphs. It is therefore not taxa (Liem, '79, '80) and has not been de- possible to determine the relative novelty of scribed in a strong durophage crushing prey the motor pattern seen in B. vetula during in the oral jaws. It is not surprising that this this behavior. Data from the Cichlidae dur- behavior involved a motor pattern distinct ing manipulation of prey attached to the sub- from that seen during suction feeding, be- strate (Liem, '79) indicate a motor pattern cause the behavior is different. However, the quite different from the one reported here, biting motor pattern used during capture of but the differences in function between the prey is indistinguishable from the activity two behaviors may make comparisons inap- pattern seen in buccal manipulation of crab propriate. prey. A quantitative analysis of these data Blowing behavior in B. vetula was usually also showed that, although the biting motor associated with the forceful expulsion of prey pattern is different from that employed dur- from the buccal cavity. This behavior was ing suction feeding, it is not different from associated with a motor pattern that could be that observed during buccal manipulation distinguished from suction feeding, bite- (Wainwright and Turingan, unpublished capture, and buccal manipulation by two fea- manuscript). tures: 1) the LOP was strongly active for Buccal manipulation of prey by B. vetula > 100 msec (or about twice as long as those following capture involves a pattern of mus- observed during the other three behaviors) cular activity that is distinct from the motor and 2) the epaxialis was the only muscle 116 R.G. TURINGAN AND P.C. WAINWRIGHT other than the dilator operculi that was ac- rium and neurocranium are greatly modified, tive during the first half of the LOP activity. largely as the sites of attachment for the In general, blowing was characterized by re- hypertrophied and subdivided adductor man- duced activity of most muscles, except the dibulae muscles. B. uetula is fully capable of protractor hyoidei, LOP, and A2 adductor effective suction feeding on soft and elusive mandibulae subdivisions that dominated the prey but employs direct biting when captur- behavior (Fig. 7D). With the exception of the ing large, hard, and substrate-attached organ- LOP, none of the cranial muscles examined isms. During buccal manipulation, prey are in this study was active in all cycles of muscu- repeatedly bitten between the jaws while rap- lar activity during the blowing behavior (Fig. idly being moved in and out of the oral cavity. 8). A blowing behavior is periodically employed Blowing in B. uetula appears to be signifi- to move prey or “spit” them out during pro- cantly different from similar behaviors re- cessing. The motor patterns associated with ported in other fishes. The motor pattern biting prey capture and blowing are distinct exhibited during “spitting out” of undesir- from the motor patterns reported for other able materials ingested with the food item percomorph fishes and are among the phylo- has been documented for the carp, Cyprinus genetically novel components of the feeding carpio (Sibbing et al., ,861,and by Lauder mechanism in B. uetula. and Lanyon (’80)for the bluegill sunfish, ACKNOWLEDGMENTS Lepomis macrochirus. In the carp, the spitting cycle starts with the mouth closed and We are grateful to D.A. Hensley for provid- subsequent expansion of the oral cavity by ing laboratory space and equipment during lowering and protruding the jaws (Sibbing et the field and anatomical examination phases al., ’86). This rostra1 expansion of the oral of this study. We thank J. Turingan and D. cavity causes water to flow anteriorly through Forestier for assistance in collecting speci- the gill slits. Opening of the mouth following mens and M. Tacher for his help in shipping adduction of the opercular series and com- live fish from Puerto Rico. B. Richard, D.A. pression of the oral cavity expels water and Hensley, and two anonymous reviewers criti- unwanted materials. No muscle activity data cally reviewed the manuscript. D. Jones aided were presented for spitting by the carp (Sib- in creating computer files for all the figures bing et al., ’86). In the bluegill sunfish, com- in this paper. Partial funds for this research pression of the buccal cavity also occurred were provided by the Office of the Associate prior to mouth opening (Lauder and Lanyon, Dean for Research, University of Puerto Rico, ’80). This behavior is associated with a motor Mayaguez, and the Lerner Gray Funds for pattern in which strong activity in the adduc- Marine Research, American Museum of Nat- tor mandibulae, geniohyoideus (=protractor ural History to R.G.T. hyoidei), and sternohyoideus all occur at the LITERATURE CITED beginning of activity in the LOP muscle. This Barel, C.D.N.(1983) Towards a constructional morphol- pattern is different from that observed in B. ogy of cichlid fishes (Teleostei, Perciformes). Neth. J. uetula during spitting and blowing; here all Zool. 33;357424. muscles except the epaxialis are active only Frazer, T.K., W.J. Linberg, and G.R. Stanton (1991) in the latest stages of the LOP activity. Thus, Predation on sand dollars by grey triggerfish, Balistes cupriscus, in the northeastern Gulf of Mexico. Bull. spitting in B. uetula appears to be associated Mar. Sci. 48:159-164. with long periods of mouth opening followed Fricke, H.W. (1971)Fische als Feinde tropischer Seeigel. by oral compression. In contrast, the bluegill Mar. Biol. 9:32%338...... sunfish compresses the oral cavity before Fricke, H.W. (1975)Losen einfacher Problerne bei einem Fisch (Freiwasser an Bulistes fuscus). Z. Tierpsych. opening its mouth. 38;18-33. In summary, the ability of B. uetula to Gregory, W.K.(1933) Fish skulls. A study of the evolu- reduce large, hard-shelled prey and to extract tion of natural mechanisms. Trans. Am. Phil. SOC. prey that firmly adhere to the substrate (e.g., 23: 75-48 1. Gosline, W.A. (1987)Jaw structures and movements in chitons) is reflected in a suite of morphologi- higher teleostean fishes. Jpn. J. Ichthyol. 34:21-32. cal and functional features of the feeding Hiatt, R.W., and D. Strassburg(1960) Ecological relation- mechanism that enhance oral biting relative ships of the fish fauna on coral reefs on Marshall to less specialized percomorph taxa. Stout, Islands. Ecol. Monogr. 30:65-127. Hobson, E.S. (1974)Feeding relationships of teleostean anteriorly oriented teeth are mounted on re- fishes on coral reefs in Kona, Hawaii. U.S. Fish. Bull. duced but sturdy jaw bones. The suspenso- 72915-1031. FEEDING MECHANISM OF BALISTES VETULA 117 Lauder, G.V. (1979) Feeding mechanisms in primitive Matsuura, K. (1979) Phylugeny of the superfamily Balk- teleosts and in the halecomorph fish Amia calua. J. toidea. Mem. Fac. Fish., Hokkaido Univ. 26:49-169. Zool. London 187543478, Mok, H.K., and S.H. Shen (1983) Osteology and phylog- Lauder, G.V. (1980) Hydrodynamics of prey capture by eny of the Squamipinnes. Spec. Publ. Taiwan Mus. teleost fishes. In D. Schneck (ed): Biofluid Mechanics 1: 1-32. 11. New York Plenum Press, pp. 161-181. Motta, P.J. (1984) Mechanics and function ofjaw protru- Lauder, G.V. (1981) Form and function: Structural anal- sion in teleost fishes: A review. Copiea 1984:l-18. ysis in evolutionary morphology. Paleobiology 7r430- Muller, M., and J.W.M. Osse (1984) Hydrodynamics of 442. suction feedingin fish. Trans. Zool. Soc. London 37:51- Lauder, G.V. (1983a) Food capture. In P.W. Webb, andD. 135. Weihs (eds): Fish Biomechanics. New York: Praeger Muller, M., J.W.M. Osse, and J.H.G. Verhagen (1982) A Press, pp. 280-311. quantitative hydrodynamical model of suction feeding Lauder, G.V. (1983b) Functional design and evolution of in fish. J. Theor. Biol. 95:49-79. the pharyngeal jaw apparatus in euteleostean fishes. J. Osse, J.W.M. (1969) Functional morphology of the head Linn. Sac. (Zool.) 77:l-38. of the perch (Perca fluuiatilis): An electromyographic Lauder, G.V. (1983~)Functional and morphological bases study. 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