Prey-capture in Pomacanthus semicirculatus (Teleostei, Pomacanthidae): functional implications of intramandibular joints in marine angelfishes
Centre for Coral Reef Biodiversity, Department of Marine Biology, James Cook University, Townsville, Queensland 4811, Australia
* Author for correspondence (e-mail: nicolai.konow{at}jcu.edu.au)
Accepted 22 February 2005
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Summary |
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Key words: feeding kinematics, biomechanics, functional morphology, mandible protrusion, suspensorial rotation, feeding mode, coral reef fish
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Introduction |
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On coral reefs, recent studies have successfully documented the
ecomorphological relationships between morphology of the feeding apparatus,
associated prey-capture kinematics, behavioural performance and feeding
ecology of both wrasses (f. Labridae)
(Westneat, 1990;
Sanderson, 1990
;
Clifton and Motta, 1998
;
Ferry-Graham et al., 2001c
,
2002
;
Hulsey and Wainwright, 2002
;
Wainwright et al., 2004
) and
butterflyfishes (f. Chaetodontidae) (Motta,
1985
,
1988
,
1989
; Ferry-Graham et al.,
2001a
,b
).
While insightful, these studies have concentrated predominantly on
ramsuction feeding taxa, a continuum of feeding modes that are
primarily associated with capture of free-living, loosely attached and/or
delicate prey (Motta, 1988
;
Sanderson, 1990
;
Wainwright et al., 2004
). Jaw
closure kinematics associated with these feeding modes are generally
considered inadequate for grabbing and dislodging firmly attached and/or
structurally resilient prey (but see
Ferry-Graham et al.,
2002
).
While a number of studies have examined structural morphology in biting
coral reef teleosts, these have focussed primarily on robust bioeroders and
more gracile herbivorous or detritivorous taxa
(Bellwood and Choat, 1990;
Purcell and Bellwood, 1993
;
Bellwood, 1994
;
Bellwood, 2003
;
Alfaro et al., 2001
;
Ferry-Graham et al., 2002
;
Streelman et al., 2002
). Such
grazing, scraping and excavating forms predominate among surgeonfishes (f.
Acanthuridae) and parrotfishes (f. Scaridae), where structural attributes of
the feeding apparatus, e.g. degree of jaw robustness or motility, reflect
microhabitat use and differential patterns of food procurement
(Bellwood and Choat, 1990
;
Purcell and Bellwood, 1993
).
However, with the exception of labrids (including some scarids)
(Alfaro et al., 2001
;
Ferry-Graham et al., 2001c
,
2002
;
Westneat, 1990
) and
tetraodontiform fishes (Turingan et al.,
1995
) relatively little functional knowledge exists for biters,
especially those that feed on structurally resilient and/or sturdily attached
prey. Considering the prevalence of biting taxa on coral reefs, the paucity of
information on both functional diversity and degree of complexity in
morphology and kinematics underlying this assortment of feeding strategies
stands out as a fundamental gap in our current understanding of feeding modes
and their functional role in coral reef ecology
(Wainwright and Bellwood,
2002
).
The gracile and usually more derived biting taxa often possess an
intramandibular joint (IMJ), a major morphological innovation that increases
morphological as well as functional complexity by decoupling the mandible into
two functional units and permitting rotation of the dentary on the articular.
This may expand jaw gape, resulting in a larger area of substratum being
contacted in each feeding event (Bellwood
and Choat, 1990; Bellwood,
1994
; Purcell and Bellwood,
1993
; Streelman et al.,
2002
). While IMJ kinematics remain unquantified, IMJ presence also
appears to be associated with changes in the orientation of the body and the
jaws to the substratum (Bellwood et al.,
2004
), as well as the curvature of substratum utilised
(Bellwood et al., 2003
).
Of the coral reef teleosts putatively labelled as biters, the marine
angelfishes (f. Pomacanthidae) form an interesting and hitherto neglected
assemblage. Although taxonomically conservative (c. 80 spp.), they
are iconic reef fishes with a circum-global distribution on tropical to
warm-temperate reefs (Allen et al.,
1998). Both pomacanthids and their well-studied sister family, the
Chaetodontidae (Burgess, 1974
)
possess bristle-shaped teeth arranged in multi-tier arrays, which may provide
exceptional gripping ability during feeding
(Motta, 1989
). Chaetodontids
are known to possess a wide range of biomechanical specialisations associated
with several trophic guilds (Motta,
1985
,
1988
; Ferry-Graham et al.,
2001a
,b
)
and a similarly wide range of trophic guilds has been inferred for
pomacanthids (Allen, 1981
;
Allen et al., 1998
;
Debelius et al., 2003
;
Bellwood et al., 2004
). While
structural information exists (Gregory,
1933
; Burgess,
1974
), the functional aspects of pomacanthid feeding morphology
and biomechanics have not been quantified
(Wainwright and Bellwood,
2002
). A recent molecular phylogeny has identified the large,
robust omnivorous members of the genus Pomacanthus as the basal
pomacanthid taxon (Bellwood et al.,
2004
). In contrast to the more derived pygmy angelfishes, which
primarily target delicate prey items, Pomacanthus species feed on
firmly attached and structurally resilient invertebrate components of the reef
biota, including poriferans, tunicates, ascidians and soft corals
(Allen, 1981
;
Allen et al., 1998
;
Debelius et al., 2003
). These
prey commonly favour confined and complex microhabitats
(Richter et al., 2001
), which
raises the question: how are structurally resilient prey items reached, seized
and dislodged from confined habitats when the large body size in
Pomacanthus (sometimes 5060 cm in total length) would appear
to hinder this foraging strategy? No previously described functional system
readily explains the microhabitat utilisation and feeding patterns of
Pomacanthus, and the present study aims to quantitatively analyse the
functional morphology, kinematics and performance characteristics of the
feeding apparatus in this basal pomacanthid taxon to investigate the
structural and functional basis of pomacanthid prey procurement. We
hypothesise that the pomacanthid feeding apparatus contains novel functional
diversity, and that the associated feeding kinematics match the diverging
pomacanthid feeding guilds. Specifically, we test if Pomacanthus has
a functional IMJ and, if so, whether intramandibular kinematics facilitates an
extended gape angle as previously suggested in other IMJ-bearing taxa.
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Materials and methods |
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Dissections, manipulations and clear staining
Specimens for dissections were euthanized by immersion in seawater with an
overdose of clove oil (Munday and Wilson,
1997), manipulated for identification of biomechanical linkages
and frozen for dissection, or fixed in buffered 10% formaldehyde for
clear-stain preparations and myology studies. Tissue clearing of fixed
specimens (N=3) involved immersion in enzymatic pre-soak detergent
(Gosztonyi, 1984
) with
subsequent KOH digestion and counter-staining for bone and cartilage, using a
protocol modified from Dingerkus and Uhler
(1977
). Fixed specimens
(N=7) were dissected to determine origin, insertion, fibre
orientation and relative prominence of muscle complexes, as well as tendon,
ligament and connective tissue morphology. Cleared and stained specimens, as
well as dissections of fresh specimens were used for manipulative studies,
qualitatively examining biomechanical mechanisms adjoining the oral jaw,
suspensorial and hyoid apparatus, with the neurocranium and pectoral girdle,
during jaw protrusion, closure and retraction. During such manipulations,
specimens were pinned to a reference grid background under a mounted digital
camera, and step-photographed while the following manipulations were carried
out (see numerical arrowhead labels for directions of manipulations in
Fig. 1B). (1)
Posterior-directed force applied to the urohyal (isthmus), imitating
contraction of the m. sternohyoideus and m. hypaxiali, contributing to
mandible depression in suction-feeders. (2) Posterior-directed force applied
to the supraoccipital crest, imitating contraction of the m. epaxialis,
causing cranial elevation and facilitating mandible protrusion in ram-feeders.
(3) Caudal rotation of the ventral opercular margin, imitating contraction of
the m. levator operculi, causing displacement of the opercular linkage,
tightening the opercular-mandibular ligament (LIM), and contributing to
mandible depression. (4) Anterodorsal displacement of the quadrate articular
articulation, imitating contraction of the m. levator arcus palatini, causing
anterior-directed suspensorial rotation, and augmenting mandible protrusion in
some ram-feeders. (5) Dorsal rotation of the dentary with the articular fully
depressed, imitating contraction of m. adductor mandibulae subsection 2 (A2),
causing jaw closure. Anatomical and biomechanical diagrams were drawn directly
from dissections using a camera lucida, or traced from digital stills of
clear-stain preparations using Corel Draw v.10. (Corel Corp.). Osteology,
myology and connective tissue nomenclature follows Winterbottom
(1974
) and Motta
(1982
).
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Live specimen husbandry and experimental design
Specimens were held in individual experimental aquaria with shelter, at
26±2°C with a 12 h:12 h L:D photoperiod and screened from external
visual stimuli with an opaque nylon cloth. All fish were acclimated for
12 weeks prior to experimentation. For provisioning as well as feeding
trials, rock oyster shells of uniform size (56 cm2 surface
area) and covered with sponge, turf algae, ascidian, tubeworm and tunicate
epifauna were collected from local coastal marine pylons. During acclimation,
specimens were trained to feed under floodlight illumination on epifauna from
shells clipped into a stainless steel crocodile beak on a steel wire shaft
mounted in a 300 g polymer base.
Prior to video recording, specimens were anaesthetised by immersion in
seawater with 1% clove oil in ethanol
(Munday and Wilson, 1997).
While anaesthetised, reflective markers were attached with cyanoacrylic
glue to the skin to provide external topographic landmarks for biomechanical
linkages in the oral jaws, suspensorium, cranium and pectoral girdle
(Fig. 1). This procedure was
completed in less than 100 s and caused no apparent stress, as specimens
typically fed vigorously shortly after recovery from anaesthesia.
Sampling and analysis of kinematics
High-speed videography was completed over a 25 day period for each
specimen, with a total of three specimens (SL=190, 245 and 330 mm;
HL=51, 63 and 85 mm) being observed. All aquaria were equipped with 2
cm2 reference grid backgrounds and illuminated with two 500 W
halogen floodlights during video recording. Specimens were presented with
attached prey in the gap between the aquarium front and the reference grid
background, to ensure the specimen was perpendicular to the lens axis, and
recorded using a JVC GR-DVL9800u digital video camera at 200 images
s1. Video sequences were captured to a PC hard drive
via a Canopus DV Raptor capture board and converted to raw AVI format
in Virtual Dub v.1.0. Five feeding events for each specimen were selected for
comprehensive analysis of feeding kinematics and to generate a performance
profile of key components of the feeding apparatus. Each frame in selected
sequences was separated to eight de-interlaced image fields, yielding stacks
of 200 TIFF images s1, which were recompiled to AVI format
in MatLab v.6.0 with resulting image stream resolution of 320x240
pixels. A further three specimens (SL=197, 241, 261 mm;
HL=55, 61, 67 mm) were recorded using a 3Com single-CCD camera at 50
images s1. Sequences were captured real-time to hard drive
using Pictureworks image recording software v. 2.0 and stored as AVI files for
analysis. As this frame rate captured 30 frames per feeding event, these
sequences were only used for analysis of excursion maxima and velocity
characteristics of feeding kinematics. All selected sequences were inspected
in Virtual Dub and cropped from feeding event start (TS)
via protrusion onset (T0) to maximum protrusion
(TMAX), bite (TB) and feeding event
conclusion (TC). Onset of bite (TMAX)
coincided with maximum jaw gape and protrusion, with time of bite
(TB), being the frame showing jaw closure onto the prey.
Sequences were submitted to analysis only if the full feeding event was
completed in focus and in lateral profile. As performance maxima were the
focus of this study, slow bites were rejected, as they appeared to result from
predator hesitation. For the latter analyses, the high-speed sequences were
subsampled at 50 images s1 for standardisation and 10
feeding events for each of the six specimens filmed were analysed for maximum
gape, maximum protrusion, and total feeding event duration
(TTOT). The contribution of body ram
(RB) and jaw ram (RJ, equalling
RB extracted from total ram, RTOT) to
prey approach were also recorded.
For the performance profile analysis, 13 reference points (Fig. 1), a target point (T) on the prey where the strike landed, and an origin reference on the grid-background (used to normalise data for image flicker and in the event of slight, unnoticed prey movement) were tracked in Movias Pro v.1.0 (Pixoft-NAC, 2002). Here, x:y coordinates were extracted for each reference point position in consecutive fields of the high-speed image stream. Visual inspection of video streams determined that protrusion duration varied more temporally than closure and retraction, and coordinate data columns from each bite were thus aligned to TB, to minimise variation in feeding kinematics. Excel macros were used to calculate vector lengths (distances between paired coordinate points) and angles between paired vectors (i.e. three coordinate points). Means ± S.E.M. of resulting values were plotted as incremental displacements (image-by-image, in 5 ms increments) of angles (Fig. 4) and linear distance (Fig. 5) between digitised points in x:y coordinate space. Onset-timing, magnitude and duration is illustrated for the following kinematic variables: total ram movement relative to the prey (RTOT), from which body-ram movement (RB) was deducted to isolate jaw-ram movement (RJ), jaw gape expansion, premaxillary protrusion, mandibular rotation and protrusion, intramandibular rotation, preopercular rotation (as a proxy for suspensorial movement), opercular rotation (as a proxy for opercular linkage displacement), cranial elevation and isthmus movement (as a proxy for hyoid depression).
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Results |
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Jaw protrusion
The hyomandibular bone and neurocranium have a synovial articulation on the
ventral sphenotic margin (filled circle in
Fig. 2A), which is associated
with prominent adductor arcus palatini (AAP) and levator arcus palatini (LAP)
musculature (Fig. 2B).
Unusually, this permits anteroposterior movement of the hyomandibular, along
with the closely associated elements of the suspensorium
(Fig. 3A,B). Meanwhile,
lateromedial expansion of the suspensorium remains comparable to other
teleosts. The pterygoid series is reduced anteriorly with the palatine loosely
suspended by connective tissue between the pterygoids and a cartilaginous pad
on the lateral ethmoid (open circle in Fig.
2A). Anteriorly directed manipulation of the
hyoidhyomandibular mechanism (4 in
Fig. 1B) results in a sliding
of the palatopterygoid complex, and anterior movement of the suspensorium
augmenting lower jaw protrusion (Fig.
3A,B). An interrupted pattern of suspensorial rotation is seen
(Fig. 1C, angle H;
Fig. 4A), with an early
rotation of 4° initiating at
TB600500 ms, preceding all other feeding
kinematics, and designating the feeding event start,
TS.
The mandible (Fig. 2A)
consists of a compact dentary with an elongated, curved ventral process, a
crescent-shaped coronoid process, and an exceptionally elongate articular,
which effectively lowers the mandiblequadrate articulation fossa, and a
distinct angular (retroarticular) bone. The articular descending
process connects to the hyoid apparatus via a stout
mandibularbasihyal ligament and to the opercular series via a
prominent interopercularmandibular ligament (LIM in
Fig. 2A); no
preopercularmandibular ligament is present. The alveolar and ascending
premaxillary processes are similarly elongate, and the laterally flattened
maxilla has a prominent internal premaxillary condyle articulating with ridges
on the premaxilla, and supported by a premaxillarymaxillary ligament
(LPM, in Fig. 2C). The
anteroventrally tapering maxillary arm
(Fig. 2A) has a reduced cranial
condyle (compared with e.g. chaetodontids;
Motta, 1982). Initial
suspensorial rotation is followed by suspensorial stasis during c.
300 ms, while the onset of mandible depression
(Fig. 1D, angle L;
Fig. 4B at
TB150 ms) augments gape expansion by rotation of
38° (TB350 ms). Gape expansion coincides
with a rotation of the operculum by
8°
(Fig. 1B, angle O;
Fig. 4C), reaching maximum
rotation around TB20 ms.
The opercular series (Fig.
2B) is formed by a vertical component, the fused operculum and
suboperculum, which are connected by an interopercular-subopercular ligament
(LIS) to the horizontally rectangular interoperculum, with a resting angle
between mandible and interoperculum (Fig.
2A) of around 60°. Prominent LOP musculature can rotate the
operculum around a synovial articulation on the dorsocaudal margin of the
hyomandibular bone (Fig. 3A),
mimicked by manipulating the ventral opercular margin, and the adjoined
interoperculum in a dorsocaudal direction (3 in
Fig. 1B). This displacement
tightens the LIM (Fig. 2A),
thereby causing mandible depression (Fig.
3A,B). As the oral jaws have a dorsally inclined resting position
(Fig. 2A), due to extensive
architectural reorganisation of the skull, the opercular series kinematics
also causes rotational protrusion of the mandible
(Fig. 3A,B). The hyoid
apparatus is flexible, with reduced protractor hyoideus, sternohyoideus and
genihyoideus musculature. Pectoral girdle rotation (measured as a proxy for
hyoid depression, Fig. 1C,
angle S) attains 6.5°, around TB65 ms,
with a prolonged duration. Similarly, the cranial articulation with the
vertebra is mobile, with a raised supraoccipital crest enlarging the insertion
surface for epaxial musculature. Cranial elevation
(Fig. 1B, angle C) exhibits a
slow and gradual increase to
11°, with a peak around
TB15 ms. In kinematics analyses, rotation in these
two mechanisms are minimal around protrusion onset, only accelerating during
the latter part of jaw protrusion. Despite the pronounced mobility in these
mechanisms, neither isolated nor simultaneous manipulation (1 and 2 in
Fig. 1B) resulted in mandible
depression. The second stage of suspensorial rotation of
4°
(Fig. 4A) further augments
mandible and premaxillary protrusion (|P| and |D|
in Fig. 1A;
Fig. 5A) and reaches maximum
rotation around TB.
Jaw closure
An intramandibular joint (IMJ) is present
(Fig. 2C), with the lateral and
medial walls of the dentary forming an articulating socket for the distal
articular ascending process. Connective tissue restrains the dentary while
allowing it to rotate on the articular, causing elevation of the tooth-bearing
dentary surface. A single tendon from the medial A2 inserts into a deep medial
fossa on the coronoid process of the dentary. No articular insertion of the A2
is present. The laterally convex, tooth-bearing surfaces of both the
premaxilla and dentary contain tightly packed arrays of bristle-shaped teeth
arranged in 57 tiers with tooth lengths decreasing posteriorly. A
ventral premaxillarymaxillary ligament (VLPM in
Fig. 2C), originating from the
lateral premaxilla, inserts lateroventrally on the maxillary arm, while a
prominent and modified articulardentarymaxillary ligament (LRDM)
connects the maxillary arm to almost the entire lateroventral surface of the
dentary, but notably, not to the articular. Dentary manipulation (5 in
Fig. 1B) causes tightening of
this ligamentous array, forcing the tooth-bearing face of the premaxilla onto
the dentary tooth face, resulting in mouth closure (Figs
1C,
3B,C), with the upper and lower
jaw teeth occluding without superior or inferior overlap
(Fig. 2C). Jaw closure
kinematics (Fig. 3B) involve
rotation of the intramandibular joint over 5 ms, attaining
30°
(Fig. 1C, angle I,
Fig. 4D), and occluding the
protruded jaws at TB.
Jaw retraction
The m. adductor mandibulae (Fig.
2B), while displaying the typical three divisions seen in
teleosts, differs in some important respects. As noted above, a single tendon
from the A2 inserts wholly on the dorsal surface of the dentary coronoid
process. The A3 insertions are displaced posteriorly, away from the dentary,
with one tendon from the ventrolateral A3 inserting in a shallow
lateral fossa, while the medial A3ß inserts on the
sesamoidarticular, which is posteriorly displaced on the medial
articular. The dorsolaterally situated A1 has two subsections: the A1
inserts onto the primordial ligament (the outer articularmaxillary
ligament, or OLRM in Fig. 2B);
the A1ß inserts in a medial fossa on the premaxillary condyle of the
maxilla. Jaw retraction (Fig.
3C) occurs with a slight lag (5 ms) after TB
(Fig. 1D, angle L;
Fig. 5A), and is associated
with a pronounced lateral head jerk. Reverse body movement at this time,
caused by pectoral fin motion, yields an additional retraction of 20%
HL from the prey (Fig.
5B). Jaw retraction kinematics is of high-velocity, encompassing
35° of mandible rotation and a linear excursion of
30% HL
over 2060 ms, to complete the feeding event at
TC.
Feeding event velocity regimes and performance
Linear excursions of gape, jaw protrusion, jaw ram and body ram are
summarised in Table 1. Mandible
protrusion (Fig. 1A,
|D|) attains about 30% HL, with subsequent
retraction of the mandible beyond the resting point accounting for the
negative protrusion values (Fig.
4E). Premaxillary protrusion
(Fig. 1A,
|P|) attains
27% HL, and occurs with an
approximately 30 ms lag from mandible protrusion. During a feeding event, body
ram, measured as the change in distance from prey to the nape
(Fig. 1A,
|RB|) accounts for a 20% HL
movement (Fig. 5B). Jaw
protrusion is initiated outside a distance of 60% HL from the prey,
and jaw-ram (Fig. 1A,
|RTOTRB|)
typically covers
30% HL. Body-ram velocities exhibit little
change throughout the feeding event (Table
1); while the changes in jaw-ram velocity are notable (as
visualised by varying curve slopes in Fig.
5B), with a slow protrusion (mean 6.4 cm s1),
fast closure (mean 16.0 cm s1), and high-velocity retraction
(mean 52.4 cm s1) during the feeding event phases
(Table 1A). The conventional
measurement of total bite duration
(TCT0) averages 450 ms,
measured using jaw protrusion as proxy
(Fig. 5A). However, when
accounting for the early excursion of the suspensorium
(Fig. 4A), mean bite duration
(TCTS) increases to about 600
ms, and sometimes approaches 750 ms (Table
2).
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Discussion |
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The intramandibular joint
In an early descriptive account, Gregory
(1933) noted "an
incipient articulation of the dentary in the lower jaw of
Angelichthyes" [Holacanthus ciliaris], but did not
elaborate on functional implications, or the presence of intramandibular
joints in other pomacanthids. In fact, intramandibular articulation may be the
most significant morphological specialisation in the feeding apparatus of
pomacanthids, with drastic consequences for feeding kinematics. Whilst bearing
strong anatomical resemblance to IMJs described in other biting taxa
(Fig. 6), the IMJ kinematics of
Pomacanthus appear to be unique. In at least two acanthurid genera
(Acanthurus and Ctenochaetus;
Purcell and Bellwood, 1993
)
and three scarid genera (Chlorurus, Hipposcarus and Scarus;
Bellwood, 1994
;
Streelman et al., 2002
), IMJ
kinematics, although unquantified, appear to increase gape expansion and
function while the jaws are retracted. In Pomacanthus, however, IMJ
kinematics produce jaw closure with the mandible maximally depressed and the
jaws at peak protrusion (Fig.
3). As a result, a distinct closing stage is added prior to the
retraction phase of the feeding event, contrasting with the feeding kinematics
in other IMJ bearers, as well as in perciform teleosts as a whole
(Table 2;
Ferry-Graham and Lauder,
2001
).
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Alternative mechanisms of mandible depression and jaw protrusion
Mandible depression kinematics in Pomacanthus appears to be driven
by opercular rotation, thus differing from many other teleosts, and especially
suction and ram-feeders, in which cranial and/or hyoid kinematics have an
early onset (Muller, 1987;
Aerts et al., 1987
;
Alfaro et al., 2001
). In more
basal fishes the cranial/hyoid mechanisms are considered functional
alternatives to the opercular linkage for initiation of mandible depression
(Lauder, 1980
;
Carroll and Wainwright, 2003
).
However, our kinematic results as well as morphological properties of the
Pomacanthus feeding apparatus suggest an inferior importance of these
mechanisms in angelfishes. The onset timing of cranial elevation is delayed
and during jaw opening the hyoid apparatus does not protrude ventrally
(anterior to the isthmus in Fig.
1) as is typically the case in suction-feeders utilising this
linkage (Motta, 1982
;
Aerts et al., 1987
).
Hyoid myology appears to be reduced compared with chaetodontids
(Motta, 1982), yet the hyoid
apparatus appears to be more flexible
(Burgess, 1974
;
Motta, 1982
). Our manipulation
studies of the Pomacanthus feeding apparatus demonstrate that the
oral jaws, suspensorium and opercular series constitute a functionally
discrete unit, with component parts being capable of generating mandible
depression, gape expansion and oral jaw protrusion/retraction. The resultant
displacements are of magnitudes comparable to those obtained in video
kinematics yet exclude input from the hyoid and cranial linkages. The observed
lag in premaxillary protrusion, suggests that premaxillary kinematics is
driven by that of the mandible, corresponding with a `type-B protrusion
mechanism' (sensu Winterbottom,
1974
; see also Motta,
1984
). Pomacanthids are unusual in having the oral jaws resting
with a dorsal inclination relative to the interoperculum, which rests at a
steep angle to the operculum (Gregory,
1933
). Articular elongation increases the mandible out-lever,
while anterior displacement of the quadrate articulation leaves the proximal
articular as a hypertrophied opening in-lever
(Fig. 6). Combined, these
traits may provide the biomechanical leverage to make opercular rotation the
primary mechanism responsible for mandible depression and premaxillary
protrusion (Anker, 1974
).
Several lines of evidence support this interpretation, including the
synchrony observed in opercular rotation and mandible depression kinematics
(Fig. 4), and the presence of
well developed LOP musculature. Most labroids (including the extreme
jaw-protruders) have an opercularmandibular resting angle around
0°, and less developed opercular musculature
(Wainwright et al., 2004;
N.K., unpublished). It is perhaps for this reason that opercular rotation has
been considered of inferior importance when compared with the role of cranial
elevation for initiation of mandible depression in teleosts
(Westneat, 1990
). Still, both
Anker (1974
) and Motta
(1982
) suggested that the
opercular mechanism provided significant input to mandible depression
initiation in several suction-feeding taxa. More recent experimental studies
on suction-feeding cichlids and centropomids have shown drastically reduced
mandible depression performance after surgical severance of the
interopercularsubopercular ligament (LIS: in
Fig. 2A) while leaving the LIM,
with the opercularhyoid connection intact
(Durie and Turingan, 2004
; R.
Turingan, personal communication). While the opercular mechanism may well
represent a functional reversal to a basal teleost mechanism, dominant in
Halecostome fishes and retained in some extant larval teleosts
(Adriaens et al., 2001
;
Lauder and Liem, 1981
), it is
noteworthy that similar opercularmandibular angles are observed in
other biting taxa (Fig. 6),
both closely (Acanthurus and Ctenochaetus) and more
distantly (Scarus) related. Given the paucity of kinematics data on
biters, it remains unclear if a functional opercular mechanism is a shared
trait among biters.
Within and between-mode performance variations
Mandible protrusion of 30% HL, as observed in
Pomacanthus, may be considered extreme, and is a rare trait in
teleosts. Such protrusion magnitude was previously only described in the
cichlid genera Petenia and Caquetaia
(Waltzek and Wainwright,
2003), the chaetodontid Forcipiger (Ferry-Graham et al.,
2001a
,b
;
Motta, 1984
), and the labrid
Epibulus (Westneat and
Wainwright, 1989
). These taxa are all ramsuction feeders,
possess extreme axial elongation of several feeding apparatus elements, and
complex suspensorial mechanisms, either based on pivoting elements
(Epibulus, Petenia and Caquetaia) or suspensorial rotation
around multiple points of flexion (Forcipiger). By comparison,
Pomacanthus has suspensorial rotation around two novel points of
flexion, contributing approximately 40% of the observed mandibular protrusion
while depression of the dorsally inclined mandible contributes the remaining
60%. Axial bone elongation in Pomacanthus, albeit less pronounced
than in other extreme jaw-protruders, is considerable in chaetodontoid terms
(Motta, 1985
,
1988
). The resultant
protrusion is of comparable magnitude to Forcipiger, for example,
which displays the most extensive axial elongation of jaw osteology known in
teleosts and three novel points of suspensorial flexion
(Table 2). In contrast, the
hyomandibularcranial articulation of scarid and acanthurid IMJ-bearers
lack anteroposterior rotation, and the palatoethmoid region shows little
flexion and no reduction. Indeed little or no mandibular protrusion has been
documented in these taxa (Purcell and
Bellwood, 1993
; Bellwood,
1994
; Motta,
1982
), while in Ctenochaetus, modest suspensorial
rotation appears to be coupled with gape angle and expansion increase rather
than mandible protrusion (Purcell and
Bellwood, 1993
).
The differences in axial bone elongation and incidence of derived
mechanisms in the feeding apparatus of Pomacanthus and other extreme
jaw-protruders may reflect diverging structural requirements of
ramsuction and biting kinematics during feeding
(Table 2). In long-jawed
ramsuction feeders, the prioritising of protrusion speed over jaw
closure force (Barel, 1983)
makes an axially elongated jaw apparatus a logical prerequisite, providing
stability in order to maintain precision during the dramatic, high-velocity
protrusion kinematics (Westneat and
Wainwright, 1989
; Waltzek and
Wainwright, 2003
). Conversely, in Pomacanthus,
peak-protruded jaw closure and jaw retraction appear to be critical feeding
kinematics. The initial suspensorial rotation stage is followed by a prolonged
stage (350 ms) of partially rotated, static posture. The second rotation
stage, occurs immediately prior to jaw closure
(TB15 ms), and coincides with maximal rotation of
the opercular-, cranial- and hyoid linkages. This late-protrusion constriction
of the feeding apparatus presumably results from contraction of opercular,
suspensorial, epaxialis and hypaxialis musculature and may serve to stabilise
the oral jaw apparatus, thereby optimising the input from A2 contraction to
dentary rotation, with a resultant direct force transmission for jaw closure.
The close apposition of the hyomandibular bars, resulting from lateromedial
skull compression, is an additional trait likely to govern bite forcefulness
(Aerts, 1991
).
Interestingly, while Pomacanthus jaw protrusion velocity is very
slow (Table 1), mandible
retraction velocity (approaching 100 cm s1) surpasses the
high-velocity jaw movements of many ram feeders
(Table 2). High retraction
velocity corresponds well with the caudal displacement of A1 and A3
insertions. This displacement also leaves the A2 as the sole muscle rotating
the dentary around the IMJ. Currently, anterior four-bar linkage models
(Westneat, 1990;
Hulsey and Wainwright, 2002
;
Wainwright et al., 2004
) as
well as models for mandibular mechanical advantage
(Turingan et al., 1995
;
Wainwright and Shaw, 1999
;
Wainwright and Bellwood, 2002
;
Bellwood, 2003
;
Wainwright et al., 2004
) do
not allow for IMJ presence (Wainwright et
al., 2004
). The transmission coefficients of jaws with an IMJ are
therefore unknown at present. However, it is noteworthy that
Pomacanthus appears to be unique among IMJ-bearing teleosts in having
the distal (dentary) portion of the IMJ equal to or longer than the proximal
(articular) portion (Fig. 6).
Whether this is causally related to pomacanthids being the only taxa with a
closing IMJ remains to be determined.
Prey dislodgement force requirements could be met via alternative
pathways, as mechanical output is not always linearly coupled with muscle
contraction (Aerts et al.,
1987). At jaw occlusion the prey is clenched between tiered
bristle tooth rows in the protruded oral jaws, potentially with considerable
gripping qualities. The protruded oral jaws appear to be stabilised in
protruded-closed configuration by a rigid frame formed by the suspensorial and
opercular rotation. A slight lag (57 ms) is observed prior to mandible
retraction. It remains to be tested if this lag represents a stage of
strain-energy storage in the m. adductor mandibulae sections involved with
mandible retraction. Such an `elastic recoil mechanism' was described in the
mandible kinematics of Astatotilapia, where the power requirement for
kinematics at the observed velocity exceeded the physical capability of
mechanical output calculated from available muscle mass
(Aerts et al., 1987
). In
Pomacanthus, cranial stabilisation during the pre-retraction lag may
be preventing jaw retraction initiation, thereby augmenting strain-energy
build-up in the A1 and A3 musculature, which is mobilised upon skull
musculature relaxation (bar the A2). Trade-offs between forcefulness and
rapidity during Pomacanthus mandible retraction, along with the
functional properties of tiered bristle tooth rows, require further
investigation. Further biomechanical modelling and tensiometry combined with
EMG appear to be the most promising avenues for future research.
Ecological implications of intramandibular joints
While the IMJ of Pomacanthus structurally resembles that found in
other biters, both the IMJ kinematics and the feeding ecology differ markedly.
Only IMJs with inferred gape-expanding kinematics have previously been
described in coral reef fishes (Fig.
6), such as the Acanthuridae
(Purcell and Bellwood, 1993),
the Scaridae (Bellwood 1994
;
Streelman et al., 2002
) and in
the blennid genus Escenius (N. Konow, unpublished). These taxa
predominately graze or scrape planar or convex substrata
(Choat and Bellwood, 1985
;
Bellwood et al., 2003
;
Depczynski and Bellwood,
2003
). Hence, IMJ presence in Pomacanthus corresponds
well with previous notions of biters exhibiting increased structural
complexity in feeding apparatus morphology in accordance with the
biomechanical challenges imposed by the substratum utilised
(Wainwright and Bellwood,
2002
). However, the unique IMJ kinematics of pomacanthids
apparently relate to distinct ecological patterns of prey-capture
(grab-and-tearing), reflecting a novel, but unquantified, pattern of
microhabitat utilisation.
The unusual IMJ kinematics may be particularly important in the larger,
spongivorous taxa, such as Pomacanthus, which prey on a wide range of
invertebrate taxa, including sponges
(Burns et al., 2003),
gorgonians (Fenical and Pawlik,
1991
) and soft corals (Wylie
and Paul, 1989
). These prey-taxa typically possess potent
predator-deterring toxins (Wylie and Paul,
1989
), leading previous workers to the assumption that chemical
defence may be the primary basis for predation deterrence in these important
components of the non-coralline benthic reef community
(Dunlap and Pawlik, 1996
).
Sponge toxin concentrations correlate well with the degree of within-habitat
exposure to predation (Swearingen and
Pawlik, 1998
). Chaetodontoid fishes appear to utilise toxic prey
through presumed tolerance of toxins
(Wylie and Paul, 1989
;
Dunlap and Pawlik, 1996
;
Gleibs and Mebs, 1999
;
Thacker et al., 1998
), but a
complementary explanation may exist: many of the less exposed (and less toxic)
invertebrate taxa also exhibit less structural resilience, and while it is
likely that chemical and structural defences work in concert to reduce
predation, as commonly seen in algae (Hay,
1992
), trade-offs may exist between toughness and crypsis for many
of the taxa consumed by pomacanthids. The result may be that the least
structurally defended species exhibit the most cryptic lifestyles, and that
the distribution and abundance of such invertebrate taxa is shaped by the
abundance of predators with jaw protrusibility, coupled with a grab and
tearing force sufficient enough to utilise such cryptobenthic resources. Other
predators robust enough to dislodge these taxa may simply be unable to reach
them due to large body size. This opens an interesting avenue of ecological
research into the relative importance of large angelfish taxa in shaping the
distribution and abundance of toxic and/or structurally resilient,
cryptobenthic reef taxa.
Microhabitat utilisation in Pomacanthus contrasts markedly with
most other coral reef fishes that feed predominantly on either free-living
(ramsuction feeders), or attached prey on convex or planar surfaces
(biters). The unique microhabitat utilisation patterns in Pomacanthus
are apparently facilitated by several unusual kinematic characteristics, all
bearing more resemblance to ram-feeders than to other biters
(Table 2). As in long-jawed
butterflyfishes, which are known to ram-feed on elusive non-attached prey in
confined microhabitats, Pomacanthus exhibit extensive oral-jaw
protrusion, enabling them to reach prey in complex and confined microhabitats.
The unique IMJ kinematics, yielding peak-protruded jaw closure, combines with
the prehensile properties of tiered bristle tooth rows, to reach concavities
and obtain a high-tenacity grip on prey. Finally, the abrupt and high-velocity
kinematics of jaw retraction, along with reverse body acceleration caused by
pectoral fin and cranial movements, generates sufficient tearing strength
and/or momentum to dislodge prey with pronounced structural resilience. These
distinct traits, coupled with the characteristic repetitive-bite foraging
pattern observed in spongivorous angelfishes suggest these taxa represent a
functionally, as well as ecologically, distinct component of reef assemblages.
Overall, the prey-capture kinematics of Pomacanthus differs markedly
from other biters and, accordingly, their feeding activity should be
considered as a new grab-and-tearing subcategory. How widespread this trait is
within the Pomacanthidae, as well as in other teleost taxa, remains to be
evaluated. However, the diversity of pomacanthid feeding guilds
(Bellwood et al., 2004)
suggests that we may find considerable functional diversity within this
family.
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Acknowledgments |
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References |
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