Evolution and Mechanics of Long Jaws inButterflyfishes (Family Chaetodontidae)Lara A. Ferry-Graham,1* Peter C. Wainwright,1 C. Darrin Hulsey,1 and David R. Bellwood2
1Section of Evolution and Ecology, University of California, Davis, California2Department of Marine Biology, James Cook University, Townsville, Queensland, Australia
ABSTRACT We analyzed the functional morphology andevolution of the long jaws found in several butterflyfishes.We used a conservative reanalysis of an existing morpho-logical dataset to generate a phylogeny that guided ourselection of seven short- and long-jawed taxa in which toinvestigate the functional anatomy of the head and jaws:Chaetodon xanthurus, Prognathodes falcifer (formerlyChaetodon falcifer), Chelmon rostratus, Heniochus acumi-natus, Johnrandallia nigrirostris, Forcipiger flavissimus,and F. longirostris. We used manipulations of fresh, pre-served, and cleared and stained specimens to develop me-chanical diagrams of how the jaws might be protruded ordepressed. Species differed based on the number of jointswithin the suspensorium. We used high-speed video anal-ysis of five of the seven species (C. xanthurus, Chel. ros-tratus, H. acuminatus, F. flavissimus, and F. longirostris)to test our predictions based on the mechanical diagrams:two suspensorial joints should facilitate purely anteriorlydirected protrusion of the lower jaw, one joint should allowless anterior protrusion and result in more depression ofthe lower jaw, and no joints in the suspensorium shouldconstrain the lower jaw to simple ventral rotation aroundthe jaw joint, as seen in generalized perciform fishes. Wefound that the longest-jawed species, F. longirostris, was
KEY WORDS: lower jaw protrusion; mobile suspenso-rium; mechanics; prey capture; morphology; function
Morphological novelties are of interest in bothecological and evolutionary contexts as they tend tochallenge our ideas about how organisms work froma mechanical standpoint and the limits to changefrom a functional point of view. Some butterflyfishesin the family Chaetodontidae have an exceptionallyelongate premaxilla and mandible (lower jaw) rela-tive to other perciform fishes. Elongate jaws arefairly widespread in the family Chaetodontidae, oc-curring in all members of the genera Forcipiger,Chelmon, and Chelmonops. Slightly elongate jawsare also found in some members of Prognathodesand even some Chaetodon. Thus, some form of jawelongation is found in half of the recognized generaof Chaetodontidae (sensu Blum, 1988; Fig. 1). How-ever, we actually know little about how the peculiartrait of elongate jaws arose, or how elongate jawsfunction.
The evolution and mechanics of short-jawed but-terflyfishes have been studied fairly extensively(Motta, 1982, 1984a,b, 1985, 1988, 1989). Butterfly-fishes typically have short, robust jaws that are used
for biting corals and other attached prey, as this isthe most common feeding mode in the family(Harmelin-Vivien and Bouchon-Navaro, 1983; Sano,1989). The jaw mechanics associated with this feed-ing mode have been described (Motta, 1985, 1989),as have the associated foraging behaviors (e.g.,Harmelin-Vivien and Bouchon-Navaro, 1983;Tricas, 1989; Cox, 1994). Zooplanktivores are lesscommon within the butterflyfishes, but short-jawedspecies have also been studied in the context of howtheir jaws function to capture mid-water prey(Motta, 1982, 1984b). Corallivorous species havepresumably retained a robust jaw, and often strongteeth, from a biting ancestor. Some zooplanktivo-
Contract grant sponsor: NSF; Contract grant number: IBN-9306672; Contract grant sponsor: the Australian Research Council.
*Correspondence to: Lara A. Ferry-Graham, Section of Evolutionand Ecology, University of California, Davis, CA 95616.E-mail: [email protected]
rous species have secondarily lost some of thesefeatures; however, species often employ behavioralmodifications to utilize novel prey (Motta, 1988,1989). In both cases, the feeding mechanism largelyresembles the generalized perciform condition in ba-sic mechanical movements.
However, in the case of species like Forcipigerlongirostris, which possesses exceptionally elongatejaws, radical modifications have occurred to thefeeding mechanism. Common names assignedwithin the general literature, such as forceps fish(see, for example, Randall, 1985; Randall et al.,1990), suggest a function of the elongate jaws simi-lar to how biting short jaws might work, except that
the jaws are longer. However, there is additionalevidence that long-jawed butterflyfishes are capableof modified feeding kinematics (Motta, 1988, 1989;Ferry-Graham et al., in review). Motta (1988) notedrotation of the suspensorium during feeding in bothForcipiger species. During feeding both the upperand lower jaws are protruded anteriorly.
Protrusion of the lower jaw is unusual in teleosts.The only other description of anteriorly directed pro-trusion of the lower jaw is for the “sling jaw” wrasseEpibulus insidiator that possesses a novel jointwithin the suspensorium that facilitates anteriortranslation of the jaw joint, and hence extensive jawprotrusion (Westneat and Wainwright, 1989; West-
Fig. 1. Phylogeny of the chaetodontid fishes. Shown is Blum’s (1988) strict-consensus tree (A) and our revised phylogeny based ona conservative recoding of Blum’s (1988) morphological character data (B). The strict-consensus tree and bootstrap tree agreed exceptfor two nodes. Shown in B is the strict-consensus tree with the addition of the two nodes that were resolved in the bootstrap tree, whichare indicated by asterisks (the bootstrap values for all nodes are given). In the strict-consensus tree these two resolved nodes were atritomy in the case of Amphichaetodon 1 the Forcipiger and Chelmon clade 1 all other butterflyfishes (bootstrap value placingAmphichaetodon ancestral to the other two clades 5 56%) and a quadritomy in the case of Forcipiger 1 Hemitaurichthys 1Heniochus 1 Johnrandallia (bootstrap value placing Forcipiger ancestral to the other three genera 5 59%). For historical accuracy wehave retained the nomenclature chosen by Blum (1988) as much as possible for the terminal taxonomic units. For reference, in hisoriginal trees Blum (1988) elevated Roa, Chaetodon, Rabdophorus, Roaps, Exornator, Lepidochaetodon, Megaprotodon, Gonochaet-odon, Tetrachaetodon, Discochaetodon, Corallochaetodon (which contains Citharodeus; see Appendix A) to the generic status but allare currently considered subgenera of Chaetodon (Allen et al., 1998), so we refer to them as such in the trees shown here with the initialC before each name. Despite its placement on the phylogeny, Parachaetodon is still afforded generic status. Prognathodes has beenelevated to generic status since Blum’s work (Allen et al., 1998). Allen et al. (1998) published the most recent publication onbutterflyfishes and did not recognize C. Roaops and C. Exornator. Allen et al. (1998) also retained C. Rhombochaetodon and C.Chaetodontops. Blum (1988) subsumed C. Rhombochaetodon in C. Exornator. Nalbant, 1971, placed C. Chaetodontops within C.Rabdophorus (a subgenus recognized by both authors), and C. Roaops Mauge and Bauchot 1984 contains all of the previous membersof C. Roa except the type specimen. The number of species in each genus/subgenus is indicated in parentheses (after Blum, 1988). Iconsare shown for select genera in each clade, demonstrating the diversity of jaw length (the jaw of each icon points to its respective nameon the phylogeny). Icons are modified after Allen et al. (1998).
121BUTTERFLYFISH JAW MECHANICS AND EVOLUTION
neat, 1990). Most fishes protrude only the upper jaw(premaxilla) when they feed and the ability of teleostfishes to protrude their upper jaw is thought to be amajor contributing factor to the success and radia-tion of the perciform fishes (Schaeffer and Rosen,1961; Alexander, 1967; Lauder, 1982, 1983; Motta,1984a). The lower jaw is typically depressed, ratherthan protruded, by rotating ventrally and anteriorlyabout the posteriorly positioned jaw joint located onthe suspensorium at the quadrate.
In this study, we extend a previous analysis ofbutterflyfish relationships (Blum, 1988). We used arevised phylogeny to make informed selections oftaxa for a comparative study across levels of mor-phological modification. As a first step towards un-derstanding the function of the long jaws in butter-flyfishes, we studied the anatomy of long-jawedspecies and short-jawed species from each of themajor clades. From these observations of jaw link-age mechanics we developed simple mechanical di-agrams of how the jaws are protruded in each spe-cies. We then compared quantitative kinematic dataobtained from high-speed video of five of these spe-cies feeding on planktonic prey with the qualitativepredictions from the diagrams. We used these to-gether to gain insight into how the long jaws func-tion in prey capture.
MATERIALS AND METHODSPhylogeny of the Chaetodontidae
We reanalyzed a modified morphological data ma-trix of 34 characters coded for 21 phenetically dis-tinct and putatively monophyletic groups in theChaetodontidae (Blum, 1988). These 21 morpholog-ically distinct groups, used as the operational taxo-nomic units (OTUs) in this analysis, were desig-nated by Blum (1988) after he examined specimensor radiographs of 86 of the approximately 120 spe-cies of Chaetodontidae. Each morphologically dis-tinct group was found to be qualitatively identicalwith respect to the morphological characters exam-ined, and these groups largely reflect existing taxo-nomic designations of genera as well as previouslydesignated subgenera within the genus Chaetodon.However, on examining the morphology Blum (1988)moved several of the species within the genus Chaet-odon into OTUs that do not reflect their widely ac-cepted subgeneric classifications (See Appendix A).Using his groups, the first objective of our reexami-nation was to reconstruct the most parsimoniousinterrelationships of the groups using a revised ma-trix and thereby test the robustness of Blum’s (1988)original evolutionary hypothesis to a different cod-ing of characters. The second objective was to pro-vide bootstrap support for the proposed relation-ships of the 21 groups within the Chaetodontidae.
Blum’s phylogenetic trees were based on highlyordered character data that we believed had thepotential to exert a strong influence on the phyloge-
netic relationships constructed (Fig. 1A). Characterordering imposes differential costs on the way char-acters are optimized on the tree (Mayden and Wiley,1992). The ordering of morphological characters im-poses specific hypotheses about the way in whichmorphological evolution occurred and could lead tocircularity since character ordering can predeter-mine the inferences of the evolutionary relation-ships under investigation (Swofford and Maddison,1992). Nine of the 34 characters used in the produc-tion of Blum’s (1988) phylogenetic hypothesis werecoded as multistate and ordered: five characters hadthree ordered states, two characters had four states,one character had five ordered states, and one char-acter in Blum’s matrix was coded as having eightordered character states. Because of the significantproportion of characters originally treated as or-dered, and the large number of states proposed forseveral of these characters, we explored the conse-quences of a different character matrix and recodedall previously ordered multistate characters as un-ordered (Appendix B).
We also eliminated all unknown character statesfrom the original matrix to increase character reso-lution and to avoid any problems associated withmissing characters (Maddison, 1993). Three cellshad previously been coded as unknown because theoriginal phylogenetic analysis combined the two out-groups, Pomacanthidae and a second outgroup com-posed of the Ephippidae, Scatophagidae, and Acan-thuroidei, and the genus Drepane, into a singlehypothetical ancestor (Blum, 1988). We separatedthe hypothetical ancestor into two distinct out-groups. This separation increased resolution inthree characters in which the two outgroups dis-played different character states (Appendix B, char-acters 21, 26, 29). In addition, we changed the codingof three character states within ingroup taxa thatwere originally treated as too ambiguous to code(Appendix B, characters 2, 15, 22). Parachaetodonexhibits uniquely derived predorsal bones and a de-rived origin of the palato-palatine ligament. Thegenus Forcipiger exhibits novel jaw and tooth mor-phology according to Blum’s character coding. Theseunique character states all occurred in characterswhich were treated as ordered in Blum’s analysis.Because of their uniquely derived condition, theywere likely difficult to place in an ordered transfor-mation series. The three character states were re-coded from unknown to apomorphic conditions forthe taxa exhibiting them.
A maximum parsimony analysis of all taxa wasconducted with Swofford’s (1993) PAUP computerpackage using the branch-and-bound algorithm tofind all most-parsimonious trees. Bootstrap analy-ses were performed on these data with PAUP using100 replicates and tree bisection and reconnection(TBR) branch swapping. Because we were interestedin the evolution of novel feeding morphology in thelong-jawed species, we also analyzed relationships
122 L.A. FERRY-GRAHAM ET AL.
among the taxa with several characters removedfrom the character matrix. We removed charactersthat are generally believed to be intimately associ-ated with the feeding apparatus of perciform fishes,including characters 10, 15, 16, 21, 22, 23, 24, and 25(see Appendix B). We then conducted a second par-simony analysis to test how much the structure ofthe tree depended on these characters and comparedthe tree to the “total evidence tree,” the tree con-structed using all of the available characters.
Gross Morphology and Linkage Models
To examine the morphology of the elongate jawsand how they differed from the jaws of other butter-flyfishes, we studied seven species: Chaetodon xan-thurus, Prognathodes falcifer (formerly Chaetodonfalcifer), Chelmon rostratus, Heniochus acuminatus,Johnrandallia nigrirostris, Forcipiger flavissimus,and F. longirostris. We used the phylogeny to informour selection of these species; thus, some prelimi-nary phylogenetic results must be mentioned here.Throughout the article we will discuss them in de-creasing order of their phylogenetic distance fromthe highly morphologically modified genus, Forcip-iger (see Fig. 1B). Each vary in jaw length and wecategorized them based on the relative length of thejaw (see Table 1). As jaw length also influenced ourselection of taxa, these preliminary results will bepresented here with our species descriptions. The
species are similar in diet and habit in that none arecoral biters and all utilize relatively soft, benthicinvertebrate prey in varying proportions (see reviewin Ferry-Graham et al., 2001).
We studied Chaetodon xanthurus (subgenus Exor-nator; Fig. 1B) as the basis of our comparison withall other chaetodontids studied. This species is con-sidered short-jawed (Table 1). We also examinedindividuals of C. striatus (subgenus Chaetodon) andC. auriga (subgenus Rabdophorus) to determine thegenerality of our observations regarding Chaetodonanatomy (Table 1). We also obtained specimens ofthe slightly long-jawed Prognathodes falcifer, whichwas previously included with the genus Chaetodon(Blum, 1988), as well as two P. aculeatus for com-parison (Table 1).
We included Chelmon rostratus in our analysis aswell. This species is a member of the putative sisterclade to the Forcipiger clade (the Chelmon clade:Chelmon 1 Chelmonops 1 Coradion; Fig. 1B), andhas moderately elongate jaws (Table 1). Note thatmoderately elongate jaws are also reported in Chel-monops within this clade. Chelmon rostratus hasbeen observed probing its jaws into crevices on thereef to procure invertebrate prey (Allen et al., 1998).
Heniochus and Johnrandallia are within the For-cipiger clade (Fig. 1B; Forcipiger 1 Hemitaurich-thys 1 Heniochus 1 Johnrandallia) but possessshort jaws (Table 1), as does Hemitaurichthys in thisclade. We studied Heniochus acuminatus and also
TABLE 1. Source and details regarding specimens used for analysis
CC1 5 commercial collector, Cairns, Australia; RD1 5 retail distributor, Sacramento, California, USA; CD1 5 commercial distributor,Sacramento, California, USA; AQ1 5 Birch Aquarium, University of California San Diego, USA; CD2 5 commercial distributor, LosAngeles, California, USA; WC 5 wild caught/killed using a pole spear and scuba.TL 5 total length; cm; OTL 5 anterior margin of orbit to tail tip; cm.Jaw: head length 5 ratio of mandible length to head length from posterior margin of opercle to anterior tip of premaxilla; not elongate,,0.50; slightly elongate, 0.50–0.59; moderately elongate, 0.60–0.79; and highly elongate, $0.80.*The number of cleared and stained specimens is a subset of the total number examined. Where possible, the same specimens werenot used for both clearing and staining and the kinematic analysis.
123BUTTERFLYFISH JAW MECHANICS AND EVOLUTION
examined single individuals of H. singularis and H.chrystostomus to determine the generality of ourfindings regarding the genus. Johnrandallia ni-grirostris is the only member of the genus Johnran-dallia and was studied to determine the generalityof our findings regarding the Forcipiger clade. Incomparison with the other species studied here, H.acuminatus takes the largest proportion of midwa-ter prey (see review in Ferry-Graham et al., submit-ted). Johnrandallia nigrirostris is known to cleanparasites off other fishes in addition to a diet ofbenthic invertebrates (Allen et al., 1998).
Forcipiger longirostris has the longest jaws knownof any butterflyfish (Motta, 1984b; Table 1). Forcip-iger flavissimus is the only other member of theForcipiger genus and has moderately elongate jaws(Table 1). We studied both Forcipiger species to ac-curately characterize the genus. Note that Forcip-iger longirostris feeds almost entirely on small ca-ridean shrimp, the most elusive prey of any of thespecies studied. Forcipiger flavissimus takes a morediverse range of mobile and attached prey, includingpolychaete setae and urchin tube feet (see review inFerry-Graham et al., submitted). Both have beenobserved probing their snouts into cracks and crev-ices on the reef (P.J. Motta, personal communica-tion). However, recent work has also refuted thenotion that the elongate jaws facilitate extreme suc-tion feeding (Ferry-Graham et al., submitted).
In each of the species the morphology was inves-tigated in fresh specimens (anesthetized or recentlydeceased) or frozen specimens, and specimens fixedin formalin and stored in 70% ethanol. Muscle ori-gins, insertions, and fiber arrangements were deter-mined from preserved specimen dissection. Speci-mens were cleared using trypsin and double-stainedusing an Alcian-blue cartilage stain and alizarin-redbone stain (Dinkerhus and Uhler, 1977). The cranialskeletal anatomy of each of the primary species wasdrawn from cleared and stained specimens with theaid of a camera lucida. Movements of joints associ-ated with jaw motion were determined through di-rect manipulation of anesthetized, thawed, andcleared and stained specimens. This combination ofinformation was used to construct mechanical dia-grams of jaw function.
Kinematic Analysis
We obtained high-speed video footage of prey cap-ture from Chaetodon xanthurus, Chelmon rostratus,Heniochus acuminatus, Forcipiger flavissimus, andF. longirostris (Table 1). All species were filmedfeeding on live brine shrimp (Artemia sp.). Forcip-iger flavissimus, Chel. rostratus, H. acuminatus, andC. xanthurus were housed at 27 6 2°C in 100-Laquaria at the University of California, Davis. Videosequences were obtained with an NAC Memrecam cidigital video system recording at 250 images s-1 (F.flavissimus) or 500 images s-1 (Chel. rostratus, H.
acuminatus, and C. xanthurus). Forcipiger longiros-tris were maintained at 23 6 2°C in 100-L aquariaat James Cook University in Townsville, Australia.Feeding sequences of this species were recorded at300 or 500 images s-1 with an Adaptive Optics Kine-view digital video system. Frame rates were selectedso that at least 20 frames per feeding sequence wereobtained. The tanks were illuminated with two600W floodlights to enhance image clarity. For pre-cise scaling during analysis, a rule was placed in thefield of view and recorded for several frames. Fishwere offered prey one or a few items at a time andallowed to feed until satiated. Filming generally oc-curred over a 2–3-day period for each individual.
We analyzed only sequences in which a lateralview of the fish could clearly be seen in the imageand the fish was perpendicular to the camera toprevent measurement error. Since several of thespecies filmed here routinely hold the mouth slightlyajar and do not increase the gape to capture prey(see Ferry-Graham et al., submitted), time zero (t0)for feeding trials was taken as the first image thatmovement of the jaws in a ventral or anterior direc-tion was detected. Sequences ended at the conclu-sion of the strike as indicated by the return of thejaw to the relaxed, prefeeding position. Four feedingsequences were analyzed from each individual ofeach of the five species.
To quantify movement of skeletal elements re-lated to protrusion of the lower jaw we digitizedpoints on the video frames and calculated severalkinematic variables from the points. The followingpoints were digitized in each video frame of eachsequence using NIH Image 1.6 for Macintosh orDidge for PC (A. Cullum, University of CaliforniaIrvine; Fig. 2): 1) the anterior tip of the premaxilla;2) the dorsalmost anterior margin of the maxilla; 3)the posterior margin of the nasal bone; 4) the dor-salmost tip of the neurocranium as approximated byexternal morphology; 5) the dorsalmost tip of thepreopercle; 6) the posteriormost margin of theopercle; 7) the dorsal margin of the insertion of thepectoral fin on the body (a reference point); 8) theanteroventral tip of the preopercle; 9) the ventral tipof the maxilla; and 10) the anterior tip of the lowerjaw (dentary). The angles calculated from these dig-itized points included (see Fig. 2C): a) the angle ofthe neurocranium relative to the body (cranial ele-vation); b) the angle of the preopercle with the neu-rocranium; c) the angle of the preopercle with thelower jaw; and d) the angle of the maxilla with thepremaxilla (maxilla rotation; all measured in de-grees). The quadrate cannot be seen externally andtherefore could not be digitized directly. But, thepreopercle is attached by ligaments along its ante-rior margin to the posterior edge of the quadrate andwas therefore constrained to follow the same path ofmotion. Changes in the angle of the preopercle withthe neurocranium and the lower jaw (angles b andc), which indicated the degree of rotation of the
124 L.A. FERRY-GRAHAM ET AL.
preopercle during prey capture, were measured asproxies for rotation of the quadrate on the hyoman-dibula (angle b), and rotation of the lower jaw on thequadrate (angle c).
The four angular variables (a–d above) were si-multaneously compared among species usingMANOVA (Statview v. 4.5). Given a significantMANOVA, post-hoc univariate ANOVA was per-formed on each of the four variables. If the ANOVAwas significant, a Fisher’s paired least significantdifference post-hoc test was used to determine whichspecies were different from one another. A singleANOVA was used to compare the displacement vari-able of maximum dentary protrusion among speciesfollowed by a Fisher’s PLSD post-hoc test. Absolutedisplacement, rather than standardized, was usedin the ANOVA.
RESULTSPhylogeny
The revised character matrix gave 10 equallymost-parsimonious trees each with 83 steps. LikeBlum’s original strict consensus tree (Fig. 1A), ouranalysis separated all taxa in Chaetodontidae intothree primary groups (Fig. 1B): 1) a clade containingthe genus Amphichaetodon; 2) a clade containing
the groups Chelmonops, Chelmon, Coradion, Forcip-iger, Hemitaurichthys, Heniochus, and Johnranda-lia; and 3) a clade containing the taxa included inthe group Chaetodon, C. Roa, Prognathodes. Thestrict consensus tree produced in this analysis dif-fered in topology from Blum’s (1988) tree in twoprimary ways (Fig. 1B). First, in Blum’s tree thegroup C. Gonochaetodon formed a trichotomy withthe group Parachaetodon 1 C. Megaprotodon andthe group C. Tetrachaetodon 1 C. Discochaetodon 1C. Corallochaetodon. In our phylogeny C.Gonochaetodon was found to be the sister group toC. Tetrachaetodon 1 C. Discochaetodon 1 C. Coral-lochaetodon, and this group of four taxa was found tobe the sister group to Parachaetodon 1 C. Megapro-todon. Second, Chelmonops, which differed inBlum’s matrix by only a single ordered characterstate from the clade Chelmon 1 Chelmonops, in ouranalysis formed a polytomy with the other two gen-era in our strict consensus tree.
The monophyly of the clade containing Chelmo-nops, Chelmon, and Coradion, as well as themonophyly of the clade composed of the four taxaForcipiger, Hemitaurichthys, Heniochus, and John-randalia both had strong bootstrap support (.96%and .88%, respectively; Fig. 1B). Chelmon, Chelmo-nops, and Coradion all shared the derived features
Fig. 2. Digitizing protocol for calculating displacements and angles achieved during prey capture: A: A sample image of Forcipigerflavissimus from the NACci high-speed video camera. B: The points used to measure the path of the lower jaw and used to determinethe angles of the preopercle with the lower jaw and the neurocranium. C: Angles that were measured. Numbered points in frame Bcorrespond to descriptions of the points digitized in the methods section of the text. Letters in frame C correspond to angular variables(see also Methods): a) cranial elevation, b) angle of the preopercle with the neurocranium, c) angle of the preopercle with the lower jaw,and d) maxilla rotation.
125BUTTERFLYFISH JAW MECHANICS AND EVOLUTION
of having only five branchiostegal rays (character 9),a novel epibranchial shape (character 13), and dif-ferent predorsal bone anatomy (character 2). Theclade of four taxa containing Forcipiger was sup-ported by unique features of the kidney (character 8)and the shape of the medial extrascapular (charac-ter 30). Although support was weak, there was sometentative evidence for Forcipiger (.59% bootstrapsupport) being placed as the sister taxon to a cladecontaining Hemitaurichthys, Heniochus, and John-randalia. Furthermore, the monophyly of a cladeuniting the seven taxa in these two clades, whichcontain the Chaetodontidae species with the longestjaws, had .85% bootstrap support. The shape of thedorsal hypohyal, the shape of the first epibranchial,the fact that the ethmoid foramen is not enclosed inthe lateral ethmoid, and the insertion of the verticalpalato-vomerine ligament onto the maxillary pro-cess (characters 12, 13, 17, and 23) all representsynapomorphies which support the monophyly ofthis group of seven taxa. The groups C. Roa andPrognathodes are moderately supported sistergroups to what has been considered the large genusChaetodon. The clade containing the rest of the taxain the family Chaetodontidae is the strongest sup-ported clade on the tree (98% bootstrap support).The arrangement of the predorsal bones, the pres-ence of anterior diverticulae on the swimbladder,the absence of vertical ridges on the anterior mes-ethmoid, the reduction of the parietal dorsoven-trally, and because the lateral escapular does notenclose the temporal canal (characters 2, 6, 20, 28,and 29, respectively) are all diagnostic of this clade.
The elimination of the eight characters intimatelyrelated to the feeding morphology reduced the num-ber of ingroup taxa in the analysis to 18. The groupChelmonops, Chelmon, and Coradion collapsed, asdid two subgenera of Chaetodon, C. Gonochaet-odon 1 C. Tetrachaetodon, leaving only two totalgroups in place of the five. The parsimony analysisproduced a tree with 48 steps. The majority of thetree topology that was recovered with all 34 charac-ters was recovered intact in this reduced characteranalysis. However, there were two differences in thetopology. There was a loss of resolution between theabove C. Gonochaetodon pair, C. Discochaetodon,and C. Corallochaetodon. In addition, Johnrandal-lia came out as the outgroup to Heniochus, Hemi-taurichthys, and Forcipiger. This difference in place-ment of Forcipiger is central to an understanding ofthe evolution of the mobile suspensorium and elon-gate jaws within this group. The remaining treetopology mirrored that of the analysis containing all34 characters.
Gross Morphology
The features of the skull and jaws that appear tobe important in functionally distinguishing Chaet-odon from the other taxa studied are related to the
suspensorial elements and their associated ligamen-tous connections. Most important of these are thepalatine, the hyomandibula, the symplectic, and thequadrate, endo-, ecto-, and metapterygoids (Fig. 3).A ligament we will refer to as the ethmopalatoen-dopterygoid ligament is robust in Chaetodon andpasses in two halves from the lateral ethmoid to theendopterygoid and from the lateral ethmoid to thepalatine (Fig. 4). The latter portion of this ligamenthas been referred to as the posterior ventromedialpalatine ligament (Blum, 1988). The lateral ethmoidcontacts both the palatine and the endopterygoidand appears to be held by short, ligamentous con-nections. The palatine and endopterygoid are fusedvia a bony suture and no anterior motion of thepalatine is detectable during jaw movement. Thereis also a vertical vomeropalatine ligament that ex-tends from the anterior process of the palatine ven-trally to the lateral surface of the vomer (sensuBlum, 1988; Fig. 4). The suspensorium is immobilein the dorsoventral plane, as seen in the generalizedperciform condition, and during jaw manipulation incleared and stained specimens the premaxilla is pro-truded while the lower jaw rotates ventrally. Prog-nathodes shares these features with Chaetodon(Figs. 3, 4).
In Chelmon rostratus the suspensorial bones areslightly reduced relative to Chaetodon (Fig. 5). Thepalatine and endopterygoid are not fused; the me-dial surface of the palatine is attached to the lateralsurface of the endopterygoid via a ligament that werefer to as the palatoendopterygoid ligament (Fig.6). A flange on the palatine passes deep into theectopterygoid, limiting rotation of the palatine atthis soft connection. There is also a ligament thatextends from the lateral ethmoid to the palatine(Fig. 6). This appears to be a modification of theethmopalatoendopterygoid ligament; one segment ofthe robust, two-part ligament found in Chaetodon.Unique to Chel. rostratus is the configuration of thevertical vomeropalatine ligament; a few thin fibersappear to extend ventrally from the anterior projec-tion of the palatine deep into the facia of the adduc-tor mandibulae muscle (Fig. 6). A posterior jointwithin the suspensorium is present between theproximal head of the hyomandibula and the neuro-cranium. This joint is present in nearly all teleostfishes (Winterbottom, 1974), but it is modified inChel. rostratus to permit motion in an anterior–posterior direction. In Chel. rostratus limited ante-rior rotation of the hyomandibula on the neurocra-nium is permitted because of the mobile connectionbetween the endopterygoid and the palatine, allow-ing the endopterygoid to slide under the palatine.The hyomandibula is able to rotate forward by about5°, along with the quadrate, symplectic, endo-, ecto-,and metapterygoid complex. This rotates the jawjoint (quadrate-articular) anteriorly, allowing thelower jaw to be protruded while also being depressedin manipulated specimens.
126 L.A. FERRY-GRAHAM ET AL.
Fig. 3. Cranial anatomy of butterflyfishes drawn from cleared and stained specimens. A: Chaetodon xanthurus. B: Prognathodesfalcifer. C: Heniochus acuminatus. D: Johnrandallia nigrirostris. The orbital bones have been cut near the neurocranium and removedand the preopercle has been removed to facilitate a view of the suspensorial elements. opc, opercle; sop, subopercle; hym, hyoman-dibula; ihy, interhyal, hyd, hyoid; mtp, metapterygoid; enp, endopterygoid; ect, ectopterygoid; qud, quadrate; sym, symplectic; iop,interopercle; par, parietal; let, lateral ethmoid; pal, palatine; nas, nasal bone; vom, vomer; max, maxilla; pmx, premaxilla; art,articular; dnt, dentary (articular 1 dentary 5 mandible or lower jaw). Scale bars are 1.0 cm.
Fig. 4. Specific aspects of the cranial anatomy of Chaetodon xanthurus. A: Ligaments associated with the suspensorium. B: Thesuperficial portion of the adductor arcus palatini muscle. C: Reduced cranial morphology illustrating jaw motion with one joint at thelower jaw. D: Reduced cranial morphology showing a medial view of the hyoid apparatus on the same side of the head (note thatstippling has been used to enhance the sections where bones are not present). eil, epihyal-interopercular ligament; epel, two-partethmopalatoendopterygoid ligament; vpl, vomeropalatine ligament; aapm, adductor arcus palatini muscle; ehy, epihyal; chy, cerato-hyal (epihyal 1 ceratohyal 5 hyoid in Fig. 3); ihy, interhyal, ect, ectopterygoid; enp, endopterygoid; mtp, metapterygoid; qud, quadrate.The fiber orientation of the adductor arcus palatini muscle is indicated by the solid lines in each diagram. In the mechanical drawingrotating joints are indicated by points and the direction of movement is indicated by arrows. Scale bars are 1.0 cm.
128 L.A. FERRY-GRAHAM ET AL.
Fig. 5. Cranial anatomy of butterflyfishes drawn from cleared and stained specimens. A: Chelmon rostratus. B: Forcipigerflavissimus. C: F. longirostris. The orbital bones have been cut near the neurocranium and removed and the preopercle has beenremoved to facilitate a view of the suspensorial elements. opc, opercle; sop, subopercle; hym, hyomandibula; ihy, interhyal, hyd, hyoid;mtp, metapterygoid; enp, endopterygoid; ect, ectopterygoid; qud, quadrate; sym, symplectic; iop, interopercle; par, parietal; let, lateralethmoid; pal, palatine; nas, nasal bone; vom, vomer; max, maxilla; pmx, premaxilla; art, articular; dnt, dentary (articular 1 dentary 5mandible or lower jaw). Scale bars are 1.0 cm.
The cranial anatomy of Johnrandallia and Henio-chus is similar. In all Johnrandallia and Heniochusexamined, the suspensorium is unmodified relative
to Chaetodon (Fig. 3). There is no evidence of pala-tine movement in manipulated specimens and a dis-tinct palatoendopterygoid ligament appears to be
Fig. 6. Specific aspects of the cranial anatomy of Chelmon rostratus. A: Ligaments associated with the suspensorium. B: Thesuperficial portion of the adductor arcus palatini muscle. C: Reduced cranial morphology illustrating jaw motion when two joints arepresent, one within the suspensorium (note that the joint between the palatine and the quadrate complex is a sliding joint). D: Reducedcranial morphology showing a medial view of the hyoid apparatus on the same side of the head (note that stippling has been used toenhance the sections where bones are not present). eil, epihyal-interopercular ligament; epel, modified ethmopalatoendopterygoidligament; pel, palatoendopterygoid ligament; vpl, vomeropalatine ligament; aapm, adductor arcus palatini muscle; ehy, epihyal; chy,ceratohyal (epihyal 1 ceratohyal 5 hyoid in Fig. 5); ihy, interhyal, ect, ectopterygoid; enp, endopterygoid; mtp, metapterygoid; qud,quadrate. In the mechanical drawing rotating joints are indicated by points and the direction of movement is indicated by arrows. Scalebars are 1.0 cm.
130 L.A. FERRY-GRAHAM ET AL.
absent. The ethmopalatoendopterygoid ligament isrobust and is in two parts, as found in Chaetodon(Fig. 4). The palatine and endopterygoid bones arelike Chaetodon. A distinct vertical vomeropalatineligament is present. Also like Chaetodon, there is noevidence of a mobile posterior joint on the suspen-sorium. The quadrate complex did not rotate ante-riorly during manipulation of the jaw in cleared andstained specimens. During jaw protrusion the lowerjaw tip rotated ventrally on the quadrate while thepremaxilla protruded anteriorly.
The suspensorial bones of Forcipiger flavissimusare reduced relative to Chaetodon and are similar inmobility to Chelmon rostratus (Fig. 5). The suspen-sorium of F. flavissimus exhibits not one joint, likeChel. rostratus, but two joints. The first of these isfunctionally similar to Chel. rostratus and is locatedanteriorly between the palatine and endopterygoid.The endopterygoid and metapterygoid bones are re-duced anteriorly and the palatine is elongate andextends posteriorly to articulate on its medial sur-face with the lateral surface of the endopterygoid atthe confluence of the endo- and ectopterygoid bones.A simple rotating joint is formed there by the pala-toendopterygoid ligament, a ligament also found inChel. rostratus. There is another robust ligamentthat extends from the ventral medial surface of thelateral ethmoid on the neurocranium to the dorsallateral surface of the endopterygoid process. Thisligament may be a modification of the ethmopala-toendopterygoid ligament; however, it is a differentmodification from that found in Chel. rostratus,where only the portion that extends from the lateralethmoid to the palatine is present. In F. flavissimusthis ligament appears to restrict motion of the pal-atine on the neurocranium relative to F. longirostris(see description of F. longirostris). A distinct verticalvomeropalatine ligament is also present that is likeChaetodon in its configuration. The second jointwithin the suspensorium is a posterior joint, likeChel. rostratus; however, this joint is between thehyomandibula and the symplectic. The hyoman-dibula lacks a solid articulation with the symplecticor the quadrate but is connected to them via softtissue. Therefore, the hyomandibula does not movewhen the jaw is protruded in manipulated speci-mens. The quadrate, symplectic, endo-, ecto-, andmetapterygoid form a complex that rotates at adorsal-medial process of the metapterygoid. An an-gle of about 10° is formed between the hyoman-dibula and symplectic as the lower jaw is protruded,rather than depressed, in manipulated cleared andstained specimens.
Cleared and stained specimen examination re-vealed that the cranial bones of Forcipiger longiros-tris appear the most anatomically extreme relativeto Chaetodon xanthurus (Fig. 5), particularly in thesuspensorium and jaws. The suspensorium of F. lon-girostris exhibits the same two joints found in F.flavissimus. The first of these is the anterior joint
between the palatine and endopterygoid. However,the endopterygoid and metapterygoid bones of F.longirostris are more reduced anteriorly relative toF. flavissimus. The palatine is elongate and extendsposteriorly to articulate on its medial surface withthe lateral surface of the endopterygoid at the con-fluence of the endo- and ectopterygoid bones. A jointis formed by the palatoendopterygoid ligament thatcan rotate a much greater degree than seen in F.flavissimus, due to the reduction of the endoptery-goid and metapterygoid bones (Fig. 7). There is alsoa vertical vomeropalatine ligament that extendsfrom the anterior process of the palatine ventrally tothe lateral surface of the vomer (Fig. 7). The pres-ence and configuration of this ligament is similar toChaetodon, but in F. longirostris the ligament ap-pears to limit anterior motion of the palatine. Thesecond joint is located posteriorly and occurs at theinterface of the hyomandibula and quadrate–symplectic complex (Fig. 7), as in F. flavissimus. Thequadrate, symplectic, endo-, ecto-, and metaptery-goid form an anteroposteriorly compressed unit thatrotates at a dorsal-medial process of the metaptery-goid as the lower jaw is protruded in manipulatedspecimens. This joint could freely rotate as much as25° in manipulated F. longirostris specimens, result-ing in extensive anterior movement of the jaw joint(quadrate-articular), and thus the lower jaw.
Examination of preserved specimens revealed amodification of the adductor arcus palatini (AAP)muscle primarily in Forcipiger longirostris (Fig. 7).The AAP originates along the basisphenoid and in-serts onto the metapterygoid, endopterygoid, andectopterygoid bones. In most perciforms, and theshort-jawed butterflyfishes, the fibers are orientedmedial-laterally (Motta, 1982; Fig. 4B). In all Henio-chus, Johnrandallia, Chelmon, and Prognathodes,like the Chaetodon studied, the fibers of the AAP areoriented medial-laterally. In F. longirostris the an-terior third of the muscle originates from theanterior-ventral region of the orbit, mostly from theethmoid bar. This portion of the AAP is considerablythicker than the posterior region. The endo- andectopterygoid bones, as indicated above, are reducedand most of the fibers of the AAP extend posteriorly,rather than laterally, to insert on the metapterygoid(behind the orbit). A few fibers of the AAP insert onthe hyomandibula (not shown in Fig. 4B). In F.flavissimus there is a slight shift in fiber orientationin the anterior portion of the muscle, but not to thedegree seen in F. longirostris. This slight shift isachieved by an extension of the dorsal margin of theendopterygoid bone that effectively extends the at-tachment site of the AAP dorsolaterally (Fig. 7).
Linkage Models
Our anatomical observations suggested that up tothree distinct joints may be involved in lower jawmotion, two of which are novel and derived within
131BUTTERFLYFISH JAW MECHANICS AND EVOLUTION
Figure 7
the Chaetodontidae. Depending on the number ofjoints present, there are different consequences forthe path of motion of the lower jaw. Chaetodon xan-thurus is used to demonstrate the condition found inall of the short-jawed butterflyfishes we studied,including Prognathodes, Heniochus, and Johnran-dallia (Fig. 4C). This condition is also found in gen-eralized perciforms. The suspensorial bones arefixed such that there is no rotation during jaw de-pression and no movement of the jaw joint. Thelower jaw rotates on the fixed quadrate and the jawrotates ventrally through an arc.
Chelmon rostratus is diagramed with intermedi-ate modifications (Fig. 6C). The hyomandibulamoves with the quadrate complex; thus, a posteriorpoint of limited rotation is at the articulation of thehyomandibula with the skull. The quadrate complexslides under the palatine due to the loose articula-tion between the two. The palatine itself is largelyfixed, but slight movement of the quadrate relativeto the palatine provides the freedom necessary forthe quadrate to rotate a small amount on the lowerjaw during depression; thus, the lower jaw movesboth anteriorly and ventrally.
Forcipiger longirostris is used to illustrate thecondition in both Forcipiger sp. There is a total ofthree joints, two in the suspensorium and one at thequadrate-articular jaw joint. Two suspensorialjoints facilitate rotation relative to the fixed neuro-cranium (Fig. 7C). The rotating quadrate complex isshown pivoting on the hyomandibula and the pala-tine. Anterior rotation of the quadrate facilitatesanterior motion of the jaw joint, and therefore pro-trusion of the lower jaw. If rotation occurs simulta-neously at the hyomandibula-metapterygoid jointand the quadrate-lower jaw joint, the lower jaw willfollow an anterior course, with little dorsal or ven-tral motion. Forcipiger flavissimus exhibits a lessmobile version of this model than F. longirostris, dueto the constraints outlined in the previous section.
Kinematic Analysis
The five species in the kinematic analysis differedonly slightly in the general behaviors related to preycapture. In each capture event the individual wouldswim around the aquarium searching for a preyitem. Detection of a prey item was indicated by adirect approach towards the brine shrimp and thenbraking, using the pectoral fins, generally with theanterior tip of the jaws within about a centimeter ofthe prey item. Although some forward locomotioncontinued due to inertia, the strike was initiatedwith the onset of lower jaw protrusion or depression(Fig. 8; t0 in sequences A–E). Peak jaw protrusion ordepression was achieved at 20–28 ms in each spe-cies (Fig. 8), after which the jaws would return totheir relaxed, prefeeding position. Failed attemptsat prey capture occurred only in the Forcipiger spe-cies and Chelmon rostratus, and were generally fol-lowed quickly by additional attempts at the sameindividual brine shrimp.
Subtle differences existed in the relative contribu-tion of rotation of the preopercle during jaw rotationand protrusion (Fig. 9). Forcipiger longirostrisshowed the greatest angular excursion of the lowerjaw on the preopercle, achieving angles upwards of20°. However, this was not significantly greaterthan the maximum angles achieved by the otherspecies, which ranged from 15–18° (Fig. 9; F4,57 51.41, P 5 0.244, power 5 0.40). Forcipiger longiros-tris exhibited a uniquely large change in the angle ofthe preopercle with the neurocranium, achieving av-erage maxima of around 12° (Fig. 9; F4,57 5 129.11,P , 0.0001, Fisher’s PLSD all P , 0.0001). Forcip-iger flavissimus achieved about 7°, which was largerthan the average maxima achieved by Chelmon ros-tratus, about 4° (Fisher’s PLSD P , 0.0001). Thissmall amount of rotation in Chel. rostratus was sig-nificantly greater than in the two short-jawed spe-cies (Fisher’s PLSD P , 0.0001), which did not ro-tate the preopercle relative to the neurocranium.
The path of motion of the lower jaw, produced bythe rotating preopercle and depression of the lowerjaw, was mostly anterior in Forcipiger longirostris(Fig. 10). Lower jaw movement was also anteriorlydirected but protruded to a significantly smallermaxima in F. flavissimus (Fig. 10; F4,57 5 22.63, P ,0.0001, Fisher’s PLSD P , 0.0001). There was amuch stronger component of ventrally directedmovement in Chelmon rostratus; however, theamount of anterior protrusion was not significantlydifferent from F. longirostris (Fisher’s PLSD P 50.111) and was significantly greater than F. flavis-simus (Fisher’s PLSD P , 0.0001). Forcipiger flav-issimus did exhibit more anterior protrusion of thelower jaw than Chaetodon xanthurus (Fisher’sPLSD P 5 0.095), which did not differ from Henio-chus acuminatus (Fisher’s PLSD P 5 0.034). Almostpurely ventrally directed movement was exhibitedby C. xanthurus and H. acuminatus (Fig. 10).
Fig. 7. Aspects of the cranial anatomy of Forcipiger longiros-tris. A: Ligaments associated with the suspensorium. B: Thesuperficial portion of the adductor arcus palatini muscle. C: Re-duced cranial morphology illustrating jaw motion when threejoints are present, two within the suspensorium. D: Reducedcranial morphology showing a medial view of the hyoid apparatusalso on the right side of the head (note that stippling has beenused to enhance the sections where bones are not present). vpl,vomeropalatine ligament; pel, palatoendopterygoid ligament; eil,epihyal-interopercular ligament; aapm, adductor arcus palatinimuscle; ehy, epihyal; chy, ceratohyal (epihyal 1 ceratohyal 5hyoid in Fig. 5); ihy, interhyal, ect, ectopterygoid; enp, endopt-erygoid; mtp, metapterygoid; qud, quadrate; pop, preopercle (notshown in other drawings). Note the compressed pterygoid ele-ments, the dorsoventrally oriented interopercle, and the anterior-posterior oriented adductor arcus palatini muscle fibers. In themechanical drawing rotating joints are indicated by points andthe direction of movement is indicated by arrows. Scale bars are1.0 cm.
133BUTTERFLYFISH JAW MECHANICS AND EVOLUTION
Fig. 8. High-speed videoframes of individuals at t0(left) and at peak jaw protru-sion (right). The time of peakjaw protrusion is noted in eachframe. Species are: (A) Chaet-odon xanthurus, (B) Chelmonrostratus, (C) Heniochusacuminatus, (D) Forcipigerflavissimus, and (E) F. lon-girostris. All events shown aresuccessful prey captures. Thebrine shrimp is still visible inthe jaws of C. xanthurus atpeak protrusion. The grids inimages B–E are 1.0 cm2.
Fig. 9. The angle of the preo-percle with the lower jaw (solidlines) and with the neurocranium(dashed lines) for: (A) Chaetodonxanthurus, (B) Chelmon rostratus,(C) Heniochus acuminatus, (D) For-cipiger flavissimus, and (E) F. lon-girostris. The angles, expressed indegrees, are shown along with thepath of motion of the mobile compo-nents on a skull of F. longirostris forreference. Note that the angle of thepreopercle with the neurocraniumis expressed as a negative excursion(see Fig. 2C; angle b). If it changesduring prey capture, this angle isreduced relative to a relaxed posi-tion at t0, while the angle of thepreopercle with the lower jaw is in-creased during feeding (Fig. 2C; an-gle c). In expressing angular excur-sions the starting value has beenstandardized to zero (prior to esti-mation of means) and all move-ments are relative to a value of zeroat t0. For each species the fourstrikes per individual were aver-aged and then an overall mean cal-culated from those individualmeans. For clarity, data from spe-cies that were analyzed at 500frames sec-1 have been subsampledso that all data shown are at 250frames sec-1.
135BUTTERFLYFISH JAW MECHANICS AND EVOLUTION
Cranial elevation was initiated at the same time aslower jaw protrusion or depression (i.e., t0); however,the contribution of cranial elevation to the strike ineach species was consistently small, with peaks be-tween 4 and 5.5° (Fig. 11; F4,57 5 0.86, P 5 0.49,power 5 0.25). Maxilla rotation generally began by 10ms into the strike and was much more variable amongspecies. Rotation was significantly larger in Forcipigerlongirostris, achieving a maximum of about 32° (Fig.11; Fisher’s PLSD all P , 0.004). Peak maxilla rota-tion occurred at approximately the same time as peakjaw protrusion or depression (see Fig. 9).
DISCUSSION
Our kinematic analysis of high-speed video foot-age revealed that Forcipiger longirostris can pro-trude its jaws in an anterior direction and to thegreatest extent, while F. flavissimus protrudes itsjaws anteriorly but to a shorter distance. Chelmonrostratus moves its jaws as much ventrally as ante-riorly. Heniochus acuminatus and Chaetodon xan-thurus exhibit an almost purely ventrally directedpath of movement of the lower jaw, with only a slightamount of protrusion occurring because the lowerjaw passes through an arc as it is depressed (Fig.10). These kinematic patterns are consistent withthe expectations of our mechanical diagrams.
With a single joint between the quadrate and thelower jaw, the tip of the lower jaw can only rotate
ventrally. Heniochus acuminatus and Chaetodon xan-thurus are unmodified from the generalized perciformcondition in this respect and their jaw movements areconstrained by a fixed suspensorium. Thus, in thesespecies the lower jaw is depressed rather than pro-truded. If, however, there are two points of rotation,the second being the quadrate on the hyomandibula orthe neurocranium, the lower jaw tip can potentiallymove anteriorly (see Fig. 7). The biomechanical modelsof Forcipiger longirostris and, to a large degree F.flavissimus, suggest that jaw protrusion can occur in amostly anterior direction, facilitated by the novel jointswithin the suspensorium. Chelmon rostratus, with itsmore intermediate modifications, should have someanterior motion of the lower jaw, but the degree of thatmotion is limited and motion should occur secondarilyin the ventral direction.
Mechanisms of Lower Jaw Protrusion
While the basic paths of movement are clear, theinput motion that causes movement of the elongatejaws of these species has not been determined di-rectly. Most lower vertebrates, including the short-jawed butterflyfish studied here (see also Motta,1982), rely primarily on the action of the sternohy-oideus muscle to depress the lower jaw through themandibulo-hyoid coupling (Winterbottom, 1974;Motta et al., 1991; Lauder and Shaffer, 1993; for anexception see Wilga and Motta, 1998). In most te-
Fig. 10. Mean path of the tip of the lower jaw asit is protruded during prey capture scaled relativeto body length of the fish (%BL). The body lengthused to scale the data was the length from theanterior margin of the orbit to the tail tip; thus, jawlength is not included in the standardization proce-dure. Species are: (A) Chaetodon xanthurus (purpleright facing triangles R), (B) Heniochus acuminatus(yellow diamonds F), (C) Chelmon rostratus (bluesquares B), (D) F. flavissimus (green circles J), and(E) Forcipiger longirostris (red upright triangles H).The starting value for each path plot has been stan-dardized to zero (prior to estimating means) and allmovements are relative to a value of zero at t0. Thedata were also rotated in coordinate space so thatthe fish body was parallel to the X-axis and antero-posterior movement of the lower jaw occurred alongthe X-axis. Values shown are the average of the fourstrikes per individual and then an overall meancalculated from those individual means. Error barsare SE; for graphical clarity only every fifth errorbar is shown.
136 L.A. FERRY-GRAHAM ET AL.
Fig. 11. Angular excursions of selected cranial elements during prey capture for: (A) Chaetodon xanthurus, (B) Chelmon rostratus,(C) Heniochus acuminatus, (D) Forcipiger flavissimus, and (E) F. longirostris. Angles are expressed as a change relative the angle att0. Change in cranial elevation is shown in solid lines and maxilla rotation in dashed lines. The angles are shown along with the pathof motion of the mobile component on a skull of F. longirostris for reference (see Fig. 2C; angles a and d). In estimating angularexcursions, the starting value has been standardized to zero (prior to estimation of means) and all movements are relative to a valueof zero at t0. Values shown are the average of the four strikes per individual and then an overall mean calculated from those individualmeans. Error bars are SE. All data shown are at 250 frames sec-1.
leosts this muscle is located on the anterior-ventralsurface of the pectoral girdle and runs forward toinsert on the urohyal which attaches to the hyoid atthe confluence of the left and right hyoid bars (Win-terbottom, 1974). The pectoral girdle is held rela-tively immobile, or retracted a small amount by theaction of the hypaxialis, so contraction of the ster-nohyoideus pulls the hyoid posteriorly. This force istransferred to the interopercle via the epihyal-interopercular ligament, which in turn puts tensionon the interoperculomandibular ligament (see alsoWestneat, 1990). The small portion of the lower jawlocated posterior to the jaw joint is pulled, causingthe jaws to pivot on the fixed quadrate (see Fig. 5).The anterior tips of the lower jaw pass through anarc as they are depressed ventrally.
With respect to jaw motion in the long-jawed but-terflyfishes this mechanism appears to present aparadox, as it would seem that sternohyoideus con-traction could not protrude the lower jaws anteriorlyinstead of depressing them ventrally. However, ourmanipulations of cleared and stained specimenssuggest a possible mechanism for sternohyoideus-powered jaw protrusion in Forcipiger. We found thatpulling posteriorly on the urohyal, simulating inputcaused by the sternohyoideus (and hyoid depres-sion), does result in forward protrusion of the lowerjaws. This action is made possible by the modifiedorientation of the hyoid bar and the interopercle inForcipiger. The hyoid and interopercle in F. lon-girostris are oriented mostly dorsoventrally ratherthan anteroposteriorly, as in more generalized taxa(see Fig. 7D). In both species of Forcipiger theepihyal-interopercular ligament is short and stout,oriented dorsoventrally, and attaches in a distinctnotch of the interopercle (Fig. 7). Posteriorly di-rected force applied to the urohyal causes the hyoidbar to continue rotating about the interhyal, placinga dorsally directed tension on the epihyal-interopercular ligament (Fig. 7). As a result of theorientation of both the ligament and the interoperclebone, the anterior-ventral tip of the interopercle isrotated dorsally. This tends to push the quadratedorsally into the skull, and because the quadratecomplex is oriented somewhat anteriorly with re-spect to its joint on the hyomandibula (see Fig. 7),the quadrate-articular joint collapses anteriorly,rather than posteriorly. Anterior rotation of thisjoint causes anterior protrusion of the lower jaw.
The ability of Forcipiger longirostris to protrudethe lower jaw anteriorly also appears to be facili-tated by the position and fiber arrangement of theadductor arcus palatini muscle (see Fig. 7B). Thechange in fiber orientation from medial-lateral toanteroposterior appears to allow the adductor arcuspalatini to rotate the pterygoid-quadrate-symplecticcomplex dorsally (Fig. 7B). Thus, the quadrate com-plex rotates at the base of the hyomandibula. As thequadrate complex is rotated, the joint between thequadrate and the lower jaw is also rotated dorsally
and anteriorly, facilitating lower jaw protrusion dur-ing prey capture.
The function of the adductor arcus palatini duringprey capture has not been experimentally measuredin butterflyfishes. However, if we are correct thatthe AAP generates the input force used for protrud-ing the lower jaw, a concomitant change in muscleactivity pattern from the generalized perciform con-dition must have occurred in Forcipiger. The AAP isusually an adductor of the suspensorium, active dur-ing the preparatory and compressive phases of preycapture (Liem, 1980; Lauder, 1983). Muscle stimu-lation experiments suggest that this adductor func-tion of the AAP is probably conserved in Chaetodon(Motta, 1982). In Forcipiger longirostris, however,the lower jaws are protruded prior to and duringactual prey entrainment. Thus, under our hypothe-sis, the AAP must be activated during the expansivephase of feeding (between the preparatory and thecompressive phases) if the AAP is involved in jawprotrusion. Thus, we predict that the AAP has anovel period of activation in F. longirostris. The AAPcannot be simultaneously responsible for both sus-pensorial adduction and jaw protrusion—the twoactivities are antagonistic. Other muscles typicallyactive with the AAP to adduct the suspensorium,such as the adductor mandibulae (Lauder, 1983),may well be sufficient to adduct the suspensorium ofF. longirostris in the absence of AAP activity.
Modifications to the AAP in the taxa studied heremay have arisen as an indirect consequence of modi-fications to the suspensorium. In Forcipiger longiros-tris, the attachment site of the AAP, the endo- andectopterygoid bones, are reduced and positioned pos-teriorly relative to the other butterflyfish taxa studied.This has the effect of causing the fibers of the AAP toextend posteriorly, rather than laterally, and resultsin a shift in fiber orientation without modifying theorigin and insertion of the muscle. In both F. flavissi-mus and Chelmon rostratus, a mostly unmodified (i.e.,medial-laterally oriented fibers) AAP could still act tofacilitate some rotation of the quadrate complex. Thequadrate complex in these two species is large andplate-like and pulling dorsally on it, where the AAPattaches, can move the quadrate dorsally, causing thejoint between the lower jaw and the quadrate to alsobe translated dorsally and the jaw to be protrudedanteriorly. In other chaetodontids the fixed quadrateprevents this motion.
Comparisons with the only other studied speciesthat exhibits anteriorly directed lower jaw protru-sion suggest a central importance of the rotatingquadrate for such jaw protrusion. In the sling-jawwrasse, Epibulus insidiator (Labridae), protrusionof the lower jaw is also achieved by the addition of ajoint in the suspensorium (Westneat and Wain-wright, 1989). A novel ligament, the vomerointero-percular ligament, transmits the motion of cranialelevation to the interopercle bone (Westneat, 1991).Rotation of the interopercle places tension on the
138 L.A. FERRY-GRAHAM ET AL.
interopercular-mandibular ligament, placing a forceat the posterior end of the lower jaw. If the quadratewere fixed, this force would cause the lower jaw torotate around the quadrate-lower jaw joint and thejaw would be depressed, as in the generalized per-ciform condition. The quadrate, however, rotates inparallel with the interopercle and the force is trans-ferred into anteriorly directed movement of thelower jaw (Westneat, 1991).
Thus, the mechanism that powers quadrate rota-tion differs in Forcipiger and Epibulus. Modifica-tions to the motion of the hyoid apparatus and to theAAP in Forcipiger have the function of cranial rota-tion in Epibulus in rotating the quadrate. However,the interopercle clearly rotates in F. longirostrisduring jaw protrusion and a sternohyoideus mecha-nism has been identified, linking interopercle rota-tion to lower jaw protrusion directly. The contribu-tion of interopercle movement combined with arotating quadrate appears to be consistent betweenForcipiger and Epibulus. It is the addition of a ro-tating quadrate, achieved by any means, that addsan “unfolding” section to the lower jaw and is thecommon feature in this convergence in function.
Evolution of Mobile Suspensoria andElongate Jaws
Blum’s (1988) phylogeny (Fig. 1A) is largely ro-bust to our conservative character coding and sub-sequent analysis of 34 characters. Only threechanges resulted from this first reanalysis. How-ever, two of these changes are important for inter-preting the evolution of the mobile suspensorium inthe species with the longest jaws. These are theplacement of Forcipiger as the outgroup to the threegenera Hemitaurichthys, Heniochus, and Johnran-dallia, and the tritomy of Coradion 1 Chelmonops(also long-jawed) 1 Chelmon for the Chelmon clade(Fig. 1B). Given this position of Forcipiger, the mo-bile suspensorium and length of the jaws may havebeen ancestral in the Forcipiger clade and lostwithin the Hemitaurichthys 1 Heniochus 1Johnrandallia clade. Alternatively, the mobile sus-pensorium and long jaws could have arisen as anovel condition within Forcipiger. This possibility iseven more likely if Johnrandallia is, in fact, thesister to the clade containing Forcipiger 1 Henio-chus 1 Hemitaurichthys as the reduced characteranalysis suggested.
Separating these two alternatives also depends onthe resolution of the polytomies present in theChelmon clade and the mobility of the suspensoriumof species within Coradion and Chelmonops. We canonly assume that Chelmonops has a mobile suspen-sorium to accompany the elongate jaws that are likeChelmon in external appearance. If Coradion is thesister taxon to Chelmonops 1 Chelmon, then parsi-mony would suggest that the mobile suspensoriumas well as long jaws evolved at least twice, once in
the Forcipiger clade and again in the Chelmon clade.If, however, Coradion is the sister taxon to one of theother two genera, as suggested by Blum’s phylogeny,then a long jaw plus mobile suspensorium could bethe ancestral character for the seven taxa in thisclade. These traits, then, would have been subse-quently lost twice (Fig. 1A), once in Coradion andagain in the Hemitaurichthys 1 Heniochus 1Johnrandallia clade (potentially more if Forcipigeris not the outgroup to this clade). A single evolutionof highly elongate jaws with a mobile suspensoriumsuggests the presence of an extant transformationseries within the Chelmon 1 Forcipiger clade. Ourreanalysis, however, finds no support for the neces-sary placement of Coradion (Fig. 1B). Resolving theChelmon polytomy will be an important step forfuture research.
Despite having slightly elongate jaws, Prognath-odes is anatomically undifferentiated from Chaet-odon in the suspensorial region (see also Blum,1988). Thus, we found no evidence of a mobile sus-pensorium and an anteriorly protruding jaw withinthe large Chaetodon branch of the phylogenetic tree(Fig. 1B). The small number of characters used ingenerating the phylogenies, however, suggests thatrelationships may change if a more extensive data-set is used. Currently the node between Chaetodonand Prognathodes is poorly supported. Additionalphylogenetic analyses may find that Prognathodes ismore appropriately placed at the base of the long-snouted clade, filling in a possible transition be-tween a short-jawed ancestor and Chelmon rostra-tus. It is equally viable given the existinginformation that Prognathodes represents an inde-pendent evolution of modified jaws without concom-itant changes to the suspensorium.
Heniochus and Johnrandallia are also morpholog-ically similar to Chaetodon. Functionally, H. acumi-natus shares the same immobile suspensorial ele-ments with C. xanthurus and both exhibit jawdepression in the manner of a generalized perciform.However, the placement of Heniochus and Johnran-dallia within the Forcipiger clade is one of the best-supported nodes on the tree. This suggests that theanatomical similarity between Chaetodon and He-niochus 1 Johnrandallia either represents a re-tained ancestral morphology or a morphology thatHeniochus 1 Johnrandallia secondarily evolvedfrom a long-jawed ancestor and structural con-straints on the skeletal system facilitate their look-ing and functioning much like Chaetodon. Giventhat the current phylogenetic evidence morestrongly supports the notion that elongate jaws andmobile suspensoria evolved independently inChelmon and Forcipiger, it is more likely that He-niochus and Johnrandallia have retained an ances-tral morphology.
Overall, we found that the longest-jawed species,Forcipiger longirostris, possesses both structuraland muscular novelties that affect the kinematics of
139BUTTERFLYFISH JAW MECHANICS AND EVOLUTION
the species and facilitate a novel pattern of move-ment, anterior protrusion of the lower jaw. The twobutterflyfish species with the moderately elongatejaws lack extreme modification and cannot protrudetheir jaws as far (in the case of F. flavissimus) or aspurely anteriorly (in the case of Chelmon rostratus).Forcipiger and Chelmon also possess slightly differ-ent solutions to the problem of creating movementwithin the suspensorium. Combined with their po-sitions on the phylogeny, this suggests that this typeof change, where the suspensorium is “freed-up,”could have occurred more than once in the family.Further understanding of the evolutionary transfor-mation to anteriorly directed jaw protrusion and amobile suspensorium will depend ultimately on theresolution of phylogenetic relationships and furtherkinematic analyses and detailed morphologicalstudy of additional members of the Chaetodontidae.
ACKNOWLEDGMENTS
The authors thank J. Grubich, A. Carroll, and D.Bolnick, as well as two reviewers, for helpful feed-back on the manuscript. P. Motta offered valuableanatomical insights and I. Hart expertly completedthe anatomical drawings. M. Foster, J. Grubich, andA. Carroll assisted with collecting video data forseveral species at UCD. We thank River City Aquat-ics and Capitol Aquarium (Sacramento, CA, USA),Quality Marine Tropicals (Los Angeles, CA, USA),B. Squire of Cairns Marine Aquarium Fish (Cairns,Australia), R. Tunin, and T. Waltzek for their coop-eration and assistance in locating specimens. F.Nosratpour and the Birch Aquarium (University ofCalifornia San Diego, La Jolla, CA, USA) providedsome particularly hard to locate specimens. R.Tunin’s knowledge and assistance with butterflyfishhusbandry was most helpful. The Adaptive Opticsvideo system used in Australia was purchased underNSF grant IBN-9306672 to PCW, and this researchwas supported by a grant from the Australian Re-search Council to DRB and PCW, and by an NSFpre-doctoral fellowship to CDH.
LITERATURE CITED
Alexander RMcN. 1967. Mechanisms of the jaws of some atheri-niform fish. J Zool Lond 151:233–255.
Allen GR, Steene R, Allen M. 1998. A guide to angelfishes andbutterflyfishes. Perth, Western Australia: Odyssey Publishing,Vanguard Press. p 250.
Blum SD. 1988. Osteology and phylogeny of the Chaetodontidae(Pisces: Perciformes). Ph.D. Dissertation. University of Hawaii,Honolulu.
Cox EF. 1994. Resource use by corallivorous butterflyfishes (Fam-ily Chaetodontidae) in Hawaii. Bull Mar Sci 54:535–545.
Dinkerhus G, Uhler LH. 1977. Enzyme clearing of Alcian bluestained whole vertebrates for demonstration of cartilage. StainTechnol 52:229–232.
Ferry-Graham LA, Wainwright PC, Bellwood DR. 2001. Preycapture in long-jawed butterflyfishes (Chaetodontidae): Thefunctional basis of novel feeding habits. J Exp Mar Biol Ecol256:167–184.
Harmelin-Vivien ML, Bouchon-Navarro Y. 1983. Feeding dietsand significance of coral feeding among chaetodontid fishes inMoorea (French Polynesia). Coral Reefs 2:119–127.
Lauder GV. 1982. Patterns of evolution in the feeding mechanismof Actinopterygian fishes. Am Zool 22:275–285.
Lauder GV. 1983. Food capture. In: Webb PW, Weihs D, editors.Fish biomechanics. New York: Praeger Publishers. p 280–311.
Lauder G, Shaffer HB. 1993. Design of feeding systems in aquaticvertebrates: major patterns and their evolutionary interpreta-tions. In: Hanken J, Hall BK, editors. The skull: functional andevolutionary mechanisms. Chicago: University of ChicagoPress. p 113–149.
Liem KF. 1980. Adaptive significance of intra- and interspecificdifferences in the feeding repertoires of cichlid fishes. Am Zool20:295–314.
Maddison WP. 1993. Missing data versus missing characters inphylogenetic analysis. Syst Biol 42:576–581.
Mayden RL, Wiley EO. 1992. The fundamentals of phylogeneticsystematics. In: Mayden RL, editor. Systematics, historicalecology, and North American freshwater fishes. Stanford: Stan-ford University Press. p 114–185.
Motta PJ. 1982. Functional morphology of the head of the inertialsuction feeding butterflyfish, Chaetodon miliaris (Perciformes,Chaetodontidae). J Morphol 174:174–283.
Motta PJ. 1984a. Mechanics and functions of jaw protrusion inteleost fishes: a review. Copeia 1–18.
Motta PJ. 1984b. Tooth attachment, replacement, and growth inbutterflyfish, Chaetodon miliaris (Chaetodontidae, Perci-formes). Can J Zool 62:183–189.
Motta PJ. 1985. Functional morphology of the head of Hawaiianand mid-Pacific butterflyfishes (Perciformes, Chaetodontidae).Env Biol Fish 13:253–276.
Motta PJ. 1988. Functional morphology of the feeding apparatusof ten species of Pacific butterflyfishes (Perciformes, Chaetodon-tidae): an ecomorphological approach. Env Biol Fish 22:39–67.
Motta PJ. 1989. Dentition patterns among Pacific and WesternAtlantic butterflyfishes (Perciformes, Chaetodontidae): rela-tionships to feeding ecology and evolutionary history. Env BiolFish 25:159–170.
Motta PJ, Hueter RE, Tricas TC. 1991. An electromyographicanalysis of the biting mechanism of the lemon shark, Negaprionbrevirostris: functional and evolutionary implications. J Mor-phol 210:55–69.
Randall JE, Allen GR, Steene RC. 1990. Fishes of the GreatBarrier Reef and Coral Sea. Bathurst, Australia: CrawfordHouse Press.
Sano M. 1989. Feeding habits of Japanese butterflyfishes (Chaet-odontidae). Env Biol Fish 25:195–203.
Schaeffer B, Rosen DE. 1961. Major adaptive levels in the evolutionof the Actinopterygian feeding mechanism. Am Zool 1:187–204.
Swofford DL. 1993. PAUP: phylogenetic analysis using parsi-mony, v. 3.1. Champaign: Illinois Natural History Survey.
Swofford DL, Maddison WP. 1992. Parsimony, character-state re-constructions, and evolutionary inferences. In: Mayden RL, editor.Systematics, historical ecology, and North American freshwaterfishes. Stanford: Stanford University Press. p 186–224.
Tricas TC. 1989. Prey selection by coral-feeding butterflyfishes:strategies to maximize the profit. Env Biol Fish 25:171–185.
Westneat MW. 1990. Feeding mechanics of teleost fishes (Labri-dae; Perciformes): a test of four-bar linkage models. J Morphol205:269–295.
Westneat MW. 1991. Linkage biomechanics and the evolution ofthe unique feeding mechanism of Epibulus insidiator (Labri-dae: Teleostei). J Exp Biol 159:165–184.
Westneat MW, Wainwright PC. 1989. Feeding mechanism ofEpibulus insidiator (Labridae; Teleostei): evolution of a novelfunctional system. J Morphol 202:129–150.
Wilga CD, Motta PJ. 1998. Feeding mechanism of the Atlanticguitarfish Rhinobatos lentiginosus: modulation of kinematicand motor activity. J Exp Biol 201:3167–3184.
140 L.A. FERRY-GRAHAM ET AL.
Winterbottom R. 1974. A descriptive synonymy of the striatedmuscles of the teleostei. Proc Acad Nat Sci Philadelphia 125:225–317.
APPENDIX A
A list of the taxa Blum (1988) examined as eitherpreserved specimens or radiographs to produce hischaracter matrix. The names under the heading rep-resent the taxa as traditionally assigned to generaand subgenera. The headings are the osteologicallydistinct taxa Blum designated and those used in ourpresent analysis. All groups currently consideredsubgenera of the genus Chaetodon are preceded by aC. Finally, because the group defined as C. Citha-roedus was ultimately identical in all characterstates to C. Corallochaetodon, only C. Corallochaet-odon was used as an endpoint for these two groupsin our analysis.
Characters which were treated as ordered in Blum’s (1988) phy-logeny. E 1 S 1 A 1 D 5 Ephippidae, Scatophagidae, Acanthu-ridae, Drepane. Taxonomic units preceded by the initial C. arecurrently considered subgenera of Chaetodon rather than genera,as suggested by Blum (1988).
Character Descriptions (Modified fromBlum, 1988)
1. First dorsal pterygiophore. (0) Simple, no but-tresses or lateral processes. (1) First dorsalspine buttressed ventrally by lateral processesof the pterygiophore. (2) First dorsal pterygio-phore with lateral processes anterior to erectordorsalis. (3) Fusion of lateral buttresses and an-terior lateral process to surround erector dorsa-lis.
2. Predorsal bones. (0) No sequential articulationbetween first dorsal pterygiophore, predorsalbones, and supraoccipital crest. (1) Sequentialarticulation between supraoccipital, predorsalbones, and first dorsal pterygiophore. (2) Firstpredorsal bone flattened and lacking posteriorgroove for second predorsal bone. (3) Single pre-dorsal bone present. (4) Heads of predorsal
bones thickened, but first retains posterodorsalgroove. (5) Similar to character state 4 but lacksposterodorsal groove.
3. Pleural rib laminae. (0) Ribs with no anteriorlaminae. (1) Weakly developed laminae. (2)Well-developed laminae.
4. Lateral line. (0) Not truncate. (1) Truncate.5. Lateral line scale count. (0) Less than 60. (1)
More than 60.6. Swimbladder. (0) With no anterior bilateral di-
verticulae. (1) With bulbous anterolateral diver-ticulae that attach to the supercleithral. (2)Swimbladder with narrow anterolateral diver-ticulae.
7. Swimbladder divided into anterior and posteriorchambers. (0) No. (1) Yes.
8. Kidney morphology. (0) Kidney not extendingbeyond first hemal spine. (1) Kidney with poste-rior bilateral lobes. (2) Bilateral lobes fusedaround first hemal spine.
9. Branchiostegal rays reduced to five. (0) No. (1)Yes.
laterally. (0) No. (1) Yes.13. First epibranchial shape in anterior view. (0)
Pomacanthidae shape. (1) Height and widthequal, the axis is inclined medially, the dorsalcartilage is wide and protrudes above the dorsalmargin, and the lateral cartilate is relativelytall. (2) The height to width ratio is 0.75, theaxis inclined medially, and all of the pieces ofcartilage are relatively small. (3) Height andwidth equal, the axis is horizontal, the medialcartilage is small, the dorsal and lateral carti-lages are wide and tall. (4) Height to width ratioless than 1.0, the axis is declined medially, themedial cartilage is larger than in all other taxa,and the dorsal and lateral cartilages are of mod-erate size.
14. Third basibranchial broad and flat. (0) Yes. (1)No.
15. Jaw and tooth morphology. (0) Outgroup mor-phology. (1) The five to ten tooth rows are posi-tioned such that there is almost always an over-lap of tooth rows within each band. (2)Maximum number of rows per tooth band is 15,five bands of teeth in jaws, disorganized tootharrangement, jaw teeth curved, produced moredorsoventrally. (3) Vertical orientation of theteeth, shortened teeth, more than three bands oftooth rows. (4) Teeth are short and straight, andless than three bands of tooth rows. (5) Jawteeth straight and long, rows short, reducedoverlap of rows. (6) All teeth on the descendingpremaxillary process absent. (7) Teeth of nearlyequivalent length, coalesced into dense brush,number of bands is increased. (8) Long-jawed
142 L.A. FERRY-GRAHAM ET AL.
but tooth rows oriented in the more commonanteromedial to posterolateral direction, the al-veoli are confined to the tip of the jaw, and threebands of tooth rows traverse the median sym-physis.
16. Vomerine teeth. (0) Well developed. (1) Partiallytoothed. (2) Toothless.
17. Ethmoid foramen completely enclosed in the lat-eral ethmoid. (0) Yes. (1) No.
20. Vertical ridges present on the anterior meseth-moid. (0) No. (1) Yes.
21. Ethmomaxillary ligament present. (0) Yes. (1) No.22. Palatopalatine ligament. (0) Originates on the
medial face of the palatine’s maxillary process.(1) Palato-palatine ligament moves posterodor-sally, some fibers originating from small apoph-ysis. (2) Apophysis well developed. (3) Originallycoded as having state 1 in Blum’s matrix (1988)but coded as unknown for character state 2.
23. Palato-vomerine ligament. (0) Two palato-vomerine ligaments not well separated. (1) Two
palato-vomerine ligaments well separated. (2)Vertical palato-vomerine ligament inserts onmaxillary process. (3) Apophysis present at in-sertion of vertical palato-vomerine ligament.
24. Basal section of the palatine is dorsoventrallynarrow and almost rod-like. (0) No. (1) Yes.
25. Ectopterygoid wide. (0) No. (1) Yes.26. Second circumorbital excluded from margin of
orbit. (0) No. (1) Yes.27. Third circumorbital with ventrally directed lam-
