Feeding ecomorphology in angelfishes, f.\ud Pomacanthidae: the implications of functional\ud innovations on prey-dislodgement in biting reef fishes

On coral reefs, biting teleosts form a major component of reef fish assemblages.\ud Nevertheless, they have been largely overlooked in functional research, while their ramsuction\ud feeding counterparts have received considerable attention over the past few\ud decades. This thesis therefore examines the functional basis of biting in coral reef fishes,\ud with a focus on the marine angelfishes (f. Pomacanthidae), and other deep-bodied\ud squamipinnid fishes.\ud To evaluate the magnitude and role of functional specialisation associated with\ud prey-capture in angelfishes, a basal species, Pomacanthus semicirculatus (Cuvier, 1931)\ud was selected as a model taxon for comprehensive functional analysis. The feeding\ud apparatus of Pomacanthus contains two biomechanical mechanisms of particular interest:\ud an intramandibular joint, and a suspensorial linkage with two novel points of flexion. Preycapture\ud kinematics were quantified using motion analysis of high-speed video, generating\ud performance profiles to illustrate timing of onset, duration and magnitude of movement in\ud the novel mechanisms. Mandible depression and suspensorial rotation coincide during jaw\ud protrusion, and augment mandible protrusion to increase head length typically by 30%.\ud Jaw closure at peak jaw protrusion appears to result from contraction of the adductor\ud mandibulae segment A2, the only segment with insertions facilitating rotation of the\ud dentary by approx. 30º relative to the articular. Feeding events are concluded by a highvelocity\ud jaw retraction typically lasting 20-50 ms, and completed in 450-750 msec.\ud Pomacanthus feeding morphology and kinematics differ from other biting teleosts, and more closely resemble some long-jawed ram-suction feeders, with the novel feeding\ud kinematics matching an unusual diet of structurally resilient and firmly attached prey.\ud Ten angelfish species representing all phylogenetic lineages were chosen from the\ud GBR fauna, in order to analyse morphological and kinematic disparity in the angelfish\ud feeding apparatus. Angelfish cranial architecture exhibits remarkable evolutionary stability\ud with constructional changes restricted to key suspensorial specialisations governing\ud increased jaw protrusibility, differential jaw protrusion angles and variations in alimentary\ud tract morphology. Whilst it was previously suggested that intramandibular joints increase\ud mechanical complexity and expand jaw-gape, in angelfishes the joint is a synapomorphy\ud with novel gape-restricting kinematics. Individual means of the 32 most informative\ud kinematics variables in Pomacanthus were extracted from high-speed video of feeding\ud events. Concordant with phylogenetic evidence, the derived pygmy-angel subgenera,\ud Centropyge [Centropyge] and C. [Xiphypops] differ significantly in several traits, whereas\ud the basal Pomacanthus subgenera are largely indistinguishable. The monotypic Pygoplites\ud exhibits the most pronounced flexion and Genicanthus consistently demonstrate the most\ud restricted flexion in most variables measured.\ud Mapping of informative alimentary traits to a phylogeny delineated divergent\ud angelfish feeding guilds. Grab-and-tearing omnivory on sponges and other sturdy prey is\ud utilised by several large and robust taxa and constitutes the basal trophic guild. More\ud gracile, biting omnivory is commonly utilised in derived pygmy-angel taxa, while\ud dislodging herbivory arose both in the basal large-bodied P. [Euxiphipops] and in the\ud derived C. [Xiphypops]; planktivory in Genicanthus is atavistic. Gape-restricting\ud intramandibular flexion, suspensorial rotation augmenting lower jaw protrusion and a high-velocity jaw retraction are important functional innovations with major implications for\ud angelfish feeding morphology and kinematics. Coupled with distinct size differences\ud amongst taxa, these traits form the functional basis for a considerable ecological\ud diversification in angelfishes.\ud The functional basis of biting in reef fishes was investigated in 11 deep-bodied\ud families, to examine the relationships between novel intramandibular joints and associated\ud trophic ecology. The results suggest convergent intramandibular joint evolution leading to\ud biting strategies in at least five families. Restricted flexion repeatedly coincides with\ud functional reversion to zoo-planktivory while basal ram-suction feeders generally lack\ud flexion. In angelfishes, intramandibular joints are symplesiomorphic and evolutionarily\ud stable, exhibiting limited kinematic divergence, averaging flexion of 27±11.1º and causing\ud jaw occlusion at peak protrusion. Angelfish kinematics contrast with all other\ud intramandibular joint bearers, in which gape-expanding flexion concludes prior to jawclosure.\ud Intramandibular flexion and transition from ram-suction to biting in butterflyfishes\ud coincide, with flexion magnitude, culminating in the crown-group of Corallochaetodon\ud (16±6.6º) and Citharoedus (49±2.7º).\ud Character mapping and optimisation revealed that up to seven intramandibular\ud flexion transitions/reversals consistently correspond with trophic transitions from freeliving\ud to attached prey. Whilst functional patterns reflect convergence of this joint, the\ud evolutionary origin of intramandibular flexion in the squamipinnid fishes remains\ud ambiguous. Nevertheless, a complex evolutionary history appears to have led to\ud widespread intramandibular joint occurrence in extant biting groups, suggesting that this is\ud a major functional innovation, and a functional prerequisite to biting in many reef fish taxa. In summary, the functional innovations of the angelfish feeding apparatus allow\ud these fishes to pass ecological thresholds and exploit novel trophic strategies, using graband-\ud tearing for herbivory and spongivory. Intramandibular joints appear to have been an\ud important functional innovation, playing a similar role in driving the ecological\ud diversification of the squamipinnes as the pharyngeal jaw apparatus in the Labroidei.\ud However, an emerging trend of reduced feeding apparatus disparity in biters, when\ud compared to ram-suction feeding taxa, supports the theory that novel traits can pose\ud constraints on functional diversification. The results herein illustrate the utility of direct\ud performance testing in quantifying disparity patterns at the organismal and assemblagelevel\ud and emphasise the potential for combining ecomorphological and biomechanical\ud techniques in elucidating the functional basis of the biting feeding mode