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First published online October 17, 2008
Journal of Experimental Biology 211, 3378-3391 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.023564
Biomechanics of a convergently derived prey-processing mechanism in fishes: evidence from comparative tongue bite apparatus morphology and raking kinematics
Department of Biology, 114 Hofstra University, Hempstead, NY 11549, USA
* Author for correspondence (e-mail: nkonow{at}jhmi)
Accepted 25 August 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: biomechanics, aquatic, feeding, behavior, fish, prey capture
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). One notable exception, pharyngeal mastication, is governed
by a functionally unique pharyngeal jaw apparatus (PJA), which decouples the
primary mandibular jaw apparatus from prey-processing tasks
(Sibbing, 1982;
Grubich, 2003;
Wainwright, 2005). The PJA is
thus mechanically and functionally distinct from the mandibular jaws
(Wainwright and Turingan,
1993; Wainwright,
2005). By contrast, most other prey-processing behaviors,
including chewing (Gillis and Lauder,
1995; Lauder,
1980; Lauder,
1981; Lauder,
1982; Sanford and Lauder,
1990), winnowing (Drucker and
Jensen, 1991) and blowing
(Turingan et al., 1995;
Turingan and Wainwright,
1993), are closely coupled with the mandibular jaws via
musculoskeletal links. The hyolingual `tongue-bite apparatus' (TBA) is a third
set of jaws situated between the oral and pharyngeal jaws in two major teleost
lineages, the osteoglossomorph and salmonid fishes
(Lauder and Liem, 1983;
Sanford and Lauder, 1989).
Given the distant relationship between these two groups
(Ishiguro et al., 2003)
(Fig. 1), the evolution of a
TBA connected to the pre-existing jaw apparatus by shared morphology may
provide an interesting model system of how coupled musculoskeletal form and
function evolve convergently to govern a derived behavioral theme
(Lauder and Reilly, 1994).
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;
Lauder and Liem, 1983)] but
absent in outgroup taxa (Fig.
1). These include (1) tooth plates or dentition on the basihyal,
which is heavily ossified; (2) directly opposing tooth plates or individual
teeth on the vomer, parasphenoid and, more laterally, the dermopalatine and
pterygoid mouth-roofing bones [together forming the tongue-bite (see
Sanford and Lauder, 1989;
Hilton, 2001)] and (3) a
cleithrobranchial ligament (CBL)
(Ridewood, 1904;
Ridewood, 1905;
Nelson, 1968;
Greenwood, 1971;
Greenwood, 1973;
Kershaw, 1976;
Taverne, 1979;
Sanford and Lauder, 1989;
Sanford and Lauder, 1990;
Sanford, 2001b;
Hilton, 2001;
Hilton, 2003). While it has
been suggested that the TBA is a convergently derived jaw apparatus
(Sanford and Lauder, 1989),
TBA morphology has never been compared between members of the two raking
lineages, which would indicate to what extent lineage-typical TBAs are
structurally equivalent. Moreover, detailed TBA morphology has only been
examined in osteoglossomorphs, where considerable structural disparity,
particularly in dentition morphology and distribution, is found
(Ridewood, 1904;
Ridewood, 1905;
Greenwood, 1973;
Taverne, 1979;
Hilton, 2003). By contrast, a
superficially conservative cranial anatomy among salmonids may reflect a
restricted TBA morphological disparity
(Lauder and Liem, 1980;
Sanford, 2000;
Sanford, 2001b).
A novel raking prey-processing behavior is directly associated with the
TBA, involving characteristic kinematics that may be ubiquitous but so far
only quantified in a phylogenetically diverse osteoglossomorph sample.
Osteoglossomorph raking kinematics divides into two categories. The first
category is primarily driven by pectoral girdle excursion and augmented by
cranial elevation, exemplified by Chitala, a notopterid knifefish
(Sanford and Lauder, 1989;
Sanford and Lauder, 1990;
Frost and Sanford, 1999). The
CBL extends medially through the sternohyoideus (SH) muscle from the pectoral
girdle to the hyoid bar and, in Chitala and other raking taxa, this
ligament may structurally duplicate the ancestral muscular connection. As
such, the CBL may provide a more direct link for translation of hypaxialis
muscle strain into basihyal retraction during raking
(Sanford and Lauder, 1989;
Hilton, 2003). By contrast,
the second category of raking is primarily driven by cranial elevation and
augmented by pectoral girdle retraction. This category is found in
Osteoglossum (silver arowana), Pantodon (African
butterflyfish) and Xenomystus (African knifefish)
(Sanford and Lauder, 1990;
Sanford, 2001a); a cranial
elevation driven pattern is also present in Salvelinus fontinalis
(brook trout), the only taxon for which there is quantitative data on salmonid
raking kinematics (Lauder and Liem,
1980; Sanford,
2001b).
Differentiation of raking kinematics from alternative prey-processing
(chewing) and functionally distinct behaviors (e.g. prey capture) within each
lineage has been thoroughly quantified
(Sanford and Lauder, 1989;
Sanford and Lauder, 1990;
Frost and Sanford, 1999;
Sanford, 2001a;
Konow et al., 2008). However,
it remains to be quantitatively demonstrated if raking is convergently derived
in the TBA-bearing lineages. The absence of similar kinematic movements
(Lauder, 1979;
Lauder, 1982;
Liem, 1990;
Sanford and Lauder, 1989) in
the feeding behavioral repertoires of outgroup teleosts, including
Amia (Lauder, 1980)
and Esox (Rand and Lauder,
1981), suggests that raking is a derived behavior
(Fig. 1;
Table 1A). Raking involves
extensive cranial elevation but also sustained oral jaw occlusion past the
preparatory phase (Table 1B).
Raking can also be divided into a distinct preparatory, power-stroke and
recovery phase, suggesting that raking resembles a (hypothetical)
`closed-mouth strike' (Sanford,
2001a; Sanford,
2001b). However, since the oral jaws are tightly occluded during
the different phases of raking (Frost and
Sanford, 1999; Sanford,
2001b), concomitant cranial elevation and pectoral girdle
retraction may result in hyoid kinematics that differ distinctly from the
typical hyoid depression generated during strikes
(Anker, 1974;
Muller, 1987;
Sanford and Wainwright, 2002).
The resulting TBA kinesis has been suggested to involve more
antero-posteriorly directed basihyal motion
(Sanford and Lauder, 1989;
Hilton, 2003), and ejected
prey debris indicates that considerable prey reduction results from the raking
power-stroke kinesis. Moreover, opercular flaring, which is commonly observed
during raking, may be caused by the hyoid bars passively abducting the
suspensorium (Muller, 1987;
Muller, 1989;
De Visser and Barel, 1996).
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Despite the interesting implications of novel raking kinematics, a lack of
muscle-activity data has, until recently, prevented determination of whether
raking is driven by a convergently derived muscle activity pattern (MAP)
(Sanford and Lauder, 1989).
This is a logical hypothesis, given the clear functional shifts from prey
capture and alternative prey-processing behaviors outlined above
(Alfaro and Herrel, 2001;
Wainwright, 2005). Raking MAP
data from the rainbow trout (Oncorhynchus mykiss) and the
osteoglossomorph arowana (Scleropages jardinii) now reveal that a
convergently derived MAP is indeed responsible for basihyal protraction and
mandibular jaw occlusion during the raking preparatory phase
(Konow and Sanford, 2008).
However, since subtle interspecific differences were present in the subsequent
raking power-stroke MAPs, exploration of the diversity in TBA morphology and
raking kinematics in these taxa is important. The ability to predict changes
in kinematics based on morphological differences is a key goal in functional
biology, and thus the TBA provides a new system for analyses of links between
organizational levels (Sanford and Lauder,
1989; Sanford and Lauder,
1990; Frost and Sanford,
1999; Sanford,
2001a; Sanford,
2001b).
Biomechanical models are valuable tools in quantitative analyses of
musculoskeletal mechanisms during teleost prey-capture
(Anker, 1974;
Muller, 1987;
Westneat, 1994;
Westneat, 1995;
Westneat, 2003;
Westneat, 2004). Conversely,
prey-processing mechanisms have generally been examined indirectly or purely
descriptively (see also Sibbing,
1982; Drucker and Jensen,
1991; Hernandez and Motta,
1997), with the exception of sciaenid pharyngeal jaw mastication,
which is a decoupled feeding mechanism
(Grubich, 2003;
Grubich, 2005;
Grubich and Westneat, 2006).
Existing prey-capture models suggest that the specific contributions of
distinct input mechanisms (e.g. cranial elevation) are important factors in
shaping the mechanistic output (i.e. basihyal motion-pattern). Thus,
biomechanical models based on TBA morphology, raking kinematics and muscle
activity in a novel musculoskeletal system (the TBA) can help identify how the
individual component mechanisms interact to shape the resulting behavior.
Our main aims are therefore to compare TBA morphology and raking kinematics
in O. mykiss and S. jardinii. These taxa have relatively
similar raking muscle activity patterns
(Konow and Sanford, 2008) and,
given evidence from their close sister taxa, they may also use relatively
similar raking kinematics (see above) (see also
Sanford and Lauder, 1990;
Sanford, 2001b). Each taxon is
a phylogenetic intermediate in its respective lineage – an advantageous
taxon pairing that may reveal subtle differences in input kinematics, which
potentially could be obscured by secondary modifications of raking kinematics
and muscle activity in alternative pairs
(Konow et al., 2008).
Specifically, we examine TBA morphology of these representatives to test the
hypothesis that the TBAs in members of the two raking lineages are
morphologically equivalent or, alternatively, that fundamental differences may
exist in TBA morphology. We compare raking input kinematics of the mandible,
hyoid, neurocranium and pectoral girdle to quantitatively test whether raking
kinematics exhibit convergent or divergent trends with the underlying
muscle-activity patterns in these taxa
(Konow and Sanford, 2008).
Comparison of raking input kinematics with those of alternative chewing
prey-processing and functionally distinct strike behaviors in both ingroup and
outgroup taxa (Amia and Esox) test whether raking kinematics
is convergently derived in the TBA-bearing lineages. Finally, we derive TBA
biomechanical models from comparative morphology, kinematics and muscle
activity evidence to obtain a theoretical framework for future quantitative
studies aiming to categorize a larger taxon sample into functional groups,
determined by the relative contribution of input mechanisms.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Specimens were housed individually at 15°C for O.
mykiss and 25°C for the three other taxa in the Hofstra University
animal care facility, in accordance with applicable ethics and animal-care
approvals. During acclimation, daily provisioning included a mix of naturally
encountered prey types, i.e. Canadian nightcrawlers (Lumbricus),
crickets (Gryllus), goldfish (Carassius) and minnows
(Pimephales), to avoid possible habituation effects on feeding
behavior. Experiments started when specimens were feeding aggressively under
floodlight illumination and otherwise appeared well acclimated.
Morphological examinations
Additional specimens (N=3 per species) were euthanized in an
alcoholic Eugenol (clove oil) overdose, used for manipulation studies, then
fixed in 10% isotonic-buffered formalin, skinned and eviscerated, and
clear-stained for bone and cartilage
(Dingerkus and Uhler, 1977).
Cleared and stained specimens were then dissected and step-photographed under
an Olympus SZX12 dissecting microscope with a digital camera. TBA diagrams
were traced from the resulting series of still images using Corel Draw v.
12.
Video recording
Specimens were video recorded whilst feeding in their home aquaria, with a
background Plexiglas grid marked in 1 cm squares for scaling purposes, located
120 mm from the front window to minimize parallax resulting from animal
movement perpendicular to the lens axis. Independent scale verification showed
the measuring error resulting from a displacement of the fish from the
background grid to the front of the tank to be <0.5 pixels. Two 600 W
floodlights provided illumination during video recording. Experimental prey
consisted of goldfish with a total length of 3–4 cm, equaling predator
mouth width. Goldfish prey were released live into the feeding arena
containing the predator, which typically caught the prey in a voracious
strike, and proceeded with prey-processing over a period ranging from 1 to 300
s before the prey was swallowed. Two days of food deprivation elapsed between
each filming event to ensure voracious predator behavior. Despite the
voracious nature of these predators, each experiment only consisted of two
feedings, since satiation affects predator performance
(Sass and Motta, 2002;
Robinson and Motta, 2002).
Therefore, feeding events were filmed over 
20 days to secure enough
digitizable sequences. Video was recorded using an NAC HSV-500 camera (Simi
Valley, CA, USA), in black and white for maximal contrast, onto super VHS
tapes at 250 frames s–1. Additional sequences were filmed
using a Photron Fastcam-X 1280 PCI camera (San Diego, CA, USA). The camera
focused on the anterior half of the fish
(Fig. 2) so that feeding head
movements could be clearly identified.
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Kinematics
Video files were batch-grabbed to PC hard drive as uncompressed (raw) AVI
files, which were then scrutinized for aberrant predator behavior, and five
representative rake sequences of each individual were selected and cropped for
analysis in Virtual Dub (v. 1.6;
http://virtualdub.org/).
In order to obtain comparable data on raking kinematics from both taxa, we
only analysed video sequences containing the preparatory, power-stroke and
recovery phases of the rake (Fig.
2). The raking power-stroke onset, or `time-zero'
(t0), was designated as one frame prior to the rapid
increase in cranial elevation, which could be easily identified among all
feeding sequences. Video sequences selected for analysis were digitized at 8
ms intervals (every second field) for 80 ms prior to, and 200 ms after,
t0 (36 frames per sequence). For all four individuals of
each taxon, five raking sequences were analyzed. Previous work has shown that
125 Hz (8 ms) is an effective sample frequency for video analysis of these
behaviors (Frost and Sanford,
1999).
The selected and cropped video files were imported to TEMA v. 2.2 (Image Systems AB, Linköping, Sweden) for data-extraction using landmark motion-tracking at frame-by-frame (8 ms) increments. In order to quantify cranial kinesis during raking (Fig. 1), the following eight landmarks were tracked: (1) the anterior upper jaw tip, (2) the anterior lower jaw tip, (3) the lower jaw (quadrate–articular) joint, (4) the dorsal and anterior-most opercular margin (morphological examinations determined that this landmark is a reliable surface proxy for the cranio-vertebral and cranio-pectoral girdle articulations), (5) the anterior-ventral corner of the orbit, (6) the body at the anterior insertion of the first dorsal fin, or alternatively an identifiable mark in the same general area, to provide a post-cranial point in the fish's frame of reference, (7) the anterior-most point of pectoral fin insertion, (8) the antero-ventral tip of the hyoid.
Resultant 2-D coordinates (x, y) from motion analysis of each
landmark were used to calculate the following four kinematic variables
(Fig. 4), describing linear and
angular displacements in the head during raking (in the fish's frame of
reference): (i) vertical gape distance, measured in cm from point 1 to 2; (ii)
hyoid distance, measured in cm as the vertical distance 5–8; we chose
this measure, as a proxy for the basihyal dorsoventral movement relative to
the ventral surface of the prey, and it may reflect compressive forces from
the TBA onto the prey; this measure does not, however, reflect the
hypothesized anteroposterior basihyal raking motion, as such movements of the
hyoid are poorly quantifiable via external motion analyses
(Sanford and Wainwright, 2002)
and are a topic for forthcoming analyses (N.K. and C.P.J.S., unpublished
data); (iii) cranial elevation, measured as the angle 5,4,6, with 4 as vertex;
this angle reflects the anterior-dorsal rotation of the TBA upper jaw during
raking; and (iv) pectoral girdle displacement after t0;
pectoral girdle displacement in the fish's frame of reference was calculated
in cm using the absolute (x,y coordinate) position at time
t1–t0 subtracted from the
reference point on the body (6). The pectoral girdle is biomechanically linked
to the lower TBA by both the SH muscle and a derived cleithrobranchial
ligament (Fig. 3). Therefore,
pectoral girdle retraction causes a posterior-directed movement of the ventral
TBA jaw. Theoretically, based on existing analyses of TBA functional
morphology (Rosen, 1974;
Lauder and Liem, 1983;
Sanford and Lauder, 1989;
Sanford and Lauder, 1990;
Sanford, 2001b), the latter
two raking kinematic components will, in synchrony, cause an opposing shearing
motion of the TBA upper and lower jaws during the raking power stroke.
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Derived variables
For each kinematic variable (Fig.
4), two derived variables were calculated, namely the magnitude of
peak displacement after t0, and the time (in ms) from
t0 to peak displacement. Since raking taxa generally
occlude their jaws during raking (Sanford
and Lauder, 1990; Sanford,
2001a; Sanford,
2001b), the peak gape displacement was actually when the
predator's gape was the smallest distance. Peak hyoid displacement reflects
maximum hyoid elevation, since the basihyal tooth plate is embedded into the
prey item during raking. Peak cranial elevation was measured when the head and
lower jaw were fully elevated during the rake
(Fig. 2). The temporal
variables were the corresponding time-to-peak values for each of the four
displacement variables. Extraction of data for the outgroup analysis of raking
kinematics, relative to strikes and chews from the ingroup and outgroup taxa,
was performed following previous methods
(Sanford, 2001b).
Statistical analyses
Descriptive statistics, including means and standard error for all eight
raking variables, were calculated (Table
2). To evaluate the overall kinematic pattern of several
variables, we used a principal component analysis (PCA) on the correlation
matrix, with PC axes constrained to four, the eigenvalues of which exceeded 1.
To examine overall inter-specific differences in raking behaviors, we ran a
multivariate analysis of variance (MANOVA) on the PCA scores, with `species'
as a fixed effect and `individuals nested within species' as a random effect.
F-ratios for the main effect of species were tested using the mean
square of individuals nested within species as the denominator
(Zar, 1999). A scatter-plot of
the informative principal component axes
(Fig. 5) was used to delineate
the taxon distribution, relative to kinematic differences.
Eigenvector-plotting of significant component loadings (>0.6)
(Table 3), scaled to PC axis
length, illustrates how the variables influenced differentiation of raking
behaviors across multivariate kinematic space.
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The outgroup analysis only differed in that the overall MANOVA used `behavior' as a fixed effect. F-ratios for the main effect of behavior were tested using the error mean square as the denominator. A significant effect of behavior would suggest that the behaviors are different irrespective of taxon. Finally, post-hoc tests using Bonferroni-corrected pairwise comparisons were used to determine if raking was distinct from both the strike and chewing behaviors.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Norden, 1961;
Rosen, 1974;
Stearley and Smith, 1993;
Sanford, 2000) and the
following description therefore focuses on morphology directly comprising the
TBA.
Mandibular jaws and the adductor mandibulae muscle
The upper oral jaws consist of a fixed premaxilla
(Fig. 3A) and a
posteroventrally tapering blade-like maxilla (not shown), both bearing single
rows of stout caniniform dentition. In resting position, the non-protrusible
mandible (Fig. 3B) lies
parallel with the body axis. It bears similar canine-like dentition and
articulates far posterior with the quadrate bone. Immediately anterior to this
articulation, the prominent m. adductor mandibulae (AM) inserts on the medial
face of the dentary via a single tendon, permitting AM contraction to
rapidly close and immobilize prey between the oral jaws.
TBA jaws and protractor hyoideus muscle
Inside the oral cavity, the upper TBA is formed by lateral dentition on the
dermopalatine (Fig. 3B), which
is ankylosed to the suspensorium yet loosely associated with the premaxilla,
maxilla and lateral ethmoid. This association allows the stout dermopalatine
tooth row to remain embedded in the prey whilst allowing some lateromedial
oral and buccal cavity kinesis during feeding. Further medial, the primary TBA
teeth occupy the anteroventral vomerine surface and extend down the vomerine
shaft (Fig. 3A) with an
anteroventrally directed tooth curvature serving to effectively impale prey as
it enters the oral cavity. In direct apposition are 6–8 posterior-curved
fangs on a short and robust basihyal, which has a hinged articulation with the
hypohyals allowing it to rotate dorsoventrally. The hyoid bar is composed of a
large anterior and posterior ceratohyal, interconnected synarthritically by
cartilage (Fig. 3B), their
lateral faces providing the posterior attachment site for the anteriorly
tapering protractor hyoideus muscle, which runs anteriorly to its attachment
onto the distal-most mandibular ramus. The hyoid bar is flexibly attached to
the distal hyomandible via the stout and short (2 mm)
interhyal.
Posterior neurocranium and epaxial musculature
The neurocranium (Fig. 3A)
has a deep and robust supraoccipital crest with a deep anterior-directed fossa
for epaxialis muscle insertion. With the cranial–vertebral joint located
far ventrally at the cranial base, epaxialis muscle contraction will
effectively rotate the neurocranium dorsally, bringing prey impaled on the
vomerine dentition forward, relative to the ventral TBA (basihyal) teeth.
Pectoral girdle and hypaxial musculature
Points of flexion exist between the supraoccipital crest and the
posttemporal, supracleithral and cleithral bones of the pectoral girdle. In
conjunction, these points of flexion facilitate anteroposterior, and also
dorsoventral, mobility of the large cleithrum but are obscured from the view
of the camera by the operculum. Therefore, manipulations of anesthetized as
well as unfixed specimens were used to estimate this dorsoventral pectoral
girdle, or intra-pectoral flexion, to approx. 25 deg.
(Fig. 3). Further distal on the
girdle, the cleithrum is ankylosed with the keel-shaped coracoid, which meets
its antimere in the midline. The posterior ramus of the coracoid provides a
surface for hypaxialis insertion and space for pectoral fin musculature.
Hypaxialis shortening will rotate the ventral pectoral girdle caudally and
retract the basihyal via the SH muscle and cleithrobranchial
ligament.
Sternohyoideus muscle and cleithrobranchial ligament
The paired SH muscle originates on the anterior coracoid face and inserts
onto a large, leaf-shaped urohyal that is attached anteriorly via a
stout ligament to the ventral hypohyal on each side. A prominent bilateral,
CBL is embedded within the SH, originating at the medial anterior tips of the
coracoid pair and extending anterodorsally towards the basihyal series
(Fig. 3A). Here, each ligament
partially attaches to a ventral cartilaginous tip of the third hypobranchial,
which has become re-orientated relative to the more horizontal hypobranchial 1
and 2 (for clarity, not shown in Fig.
3A). From here, a major portion of the ligament then extends
directly anterior and inserts onto the ventral aspect of the first
basibranchial, resulting in an arc-shaped CBL shape.
TBA morphology in S. jardinii
Osteoglossid cranial morphology has previously been described extensively
(Greenwood, 1971;
Greenwood, 1973;
Hilton, 2003) and herein we
present only those traits (Fig.
3C) that vary from O. mykiss (see above).
Mandibular jaws
The mandible in S. jardinii is longer and delineates a
lateromedially compressed oral cavity and a distinct trap-door mouth with a
dorso-oblique incline (Fig. 2).
Both mandible and maxilla have correspondingly longer rows of caniniform
dentition.
TBA jaws and protractor hyoideus muscle
The elongation of oral dentition rows transform to dentition on the
dermopalatine and the suspensorium, which is tightly associated with the
neurocranium, both at the ethmoid and sphenoid regions. Upper medial TBA
dentition is restricted to two separate sets of caniniform teeth on the
anterior and posterior-most ventral parasphenoid. Meanwhile, extensive stout
papilliform dentition forms a tooth plate on the medial endopterygoid face.
Correspondingly, a long and slender tooth plate with dense papilliform
dentition overlies the basihyal, dorsal hypohyal and basibranchials 1–3,
while the basihyal–ceratohyal–interhyal–hyomandibular series
resembles the series in O. mykiss.
Post-cranial morphology
The supraoccipital crest is low-rising and narrow with a shallow fossa
providing restricted insertion space for the epaxialis musculature, segments
of which also insert onto the posttemporal and supracleithral bones. While the
pectoral girdle has the same articulations as in O. mykiss,
manipulations showed that intra-pectoral flexion was less pronounced
(10±2 deg.), yet the ventral girdle provides larger surfaces for
posterior hypaxialis and anterior SH attachment than in O.
mykiss.
Sternohyoideus muscle and cleithrobranchial ligament
The SH muscle is relatively slender and tapers off towards the anterior
insertion onto a small sesamoid urohyal. While the cleithrobranchial ligament
originates bilaterally at locations similar to those in O. mykiss,
the ligament is more robust in S. jardinii and inserts entirely onto
a bony process of the third hypobranchial and not onto the prominent styloid
process of the second hypobranchial
(Hilton, 2001), which forms an
attachment site for at least some SH muscle fibers.
Raking kinematics
Raking is initiated with a preparatory phase at –30 ms in O.
mykiss (Movie 1 in supplementary material) and at –70 ms in S.
jardinii (Movie 2 in supplementary material), with abrupt mandibular jaw
occlusion (Fig. 2A,G). In
S. jardinii, distinct and unique cranial depression kinematics
(Fig. 2H;
Fig. 3C), in conjunction with
pectoral girdle protraction (Fig.
2H; Fig. 3D), also
begins early at –70 to –30 ms. The lower jaw is elevated prior to
t0, followed by depression, which starts and peaks
earliest in O. mykiss. The externally visible hyoid motion (point 8
in Fig. 2A,G;
Fig. 4B) appears minimal in
both taxa (0.1 cm; Table
2); however, prior to t0, a detectable gradual
elevation of the hyoid in S. jardinii ends at the onset of the power
stroke (t0) (Fig.
2H; Fig. 4B). The
raking power stroke begins with the onset of cranial elevation
(t0) (Fig.
2B,I; Fig. 4D) and
is accompanied in both taxa by the onset of pectoral girdle retraction. Both
cranial elevation and pectoral girdle retraction in O. mykiss are
approximately double that in S. jardinii
(Table 2). Interestingly,
maximum cranial elevation and pectoral girdle retraction occur at
approximately the same time (44 ms) in O. mykiss, while in S.
jardinii maximum cranial elevation occurs after maximum pectoral girdle
retraction (50±2.55 ms and 38±5.17 ms, respectively). Overall,
cranial and pectoral girdle movements are greater and (with the exception of
the pectoral girdle) faster in O. mykiss
(Fig. 4;
Table 2) while the raking
preparatory phase in S. jardinii is more complex.
A PCA on the correlation matrix from the kinematic dataset returned four
axes with eigenvalues exceeding one, together explaining 76% of the dataset
variance (28%, 20%, 15% and 13%, respectively). While a MANOVA found overall
significant differences in the dataset (Wilk's 
=0.227;
F4,30=25.527; P<0.001), a significant species
effect was only evident along axes PC2 and PC3, accounting for a total of 28%
of the variation (Table 3).
Five of the eight kinematic variables along these axes had component loadings
over 0.6 (Table 3), indicating
that they were influential in taxon separation. Nevertheless, a scatter plot
of PC2 and PC3 (Fig. 5) shows
extensive species polygon overlap in multidimensional kinematic space. The
spread of cases in this plot also shows that raking behaviors in S.
jardinii are more variable while raking is more stereotypical in O.
mykiss. Cranial elevation amplitude loaded significantly along PC3, being
almost double in O. mykiss (22.41±1.62 deg.) compared with
S. jardinii (13.05±1.45 deg.)
(Fig. 4; Tables
2 and
3), as well as reaching a peak
earlier in O. mykiss than in S. jardinii
(Table 2). Pectoral girdle
retraction was much greater but peaked later in O. mykiss than in
S. jardinii (7.5 mm and 44.3 s vs 4.1 mm and 38.2 ms).
Despite minimal hyoid movements in both taxa, hyoid elevation was more
prominent in S. jardinii during almost the entire raking behavior
(Fig. 4), and minimum gape
distance occurred significantly later in S. jardinii
(Table 2). It is noted,
however, that the latter two variables exerted less influence on taxon
segregation than the first three, as indicated by their vector planes being
perpendicular to the major segregation axis of species polygons in
Fig. 5.
General feeding kinematics
A PCA on the correlation matrix of a dataset including strike and chewing
kinematics from all four taxa and raking kinematics from the ingroups
recovered three PC axes with eigenvalues exceeding one, which explained 39%,
26% and 13% of the total dataset variance, respectively. A MANOVA recovered
statistically significant behavioral differences in the dataset (Wilk's
=0.201; F16,126=9.692; P<0.001).
Subsequent ANOVAs on the PC factor scores revealed that all axes contained
statistically significant differences in behavior
(F2,75=13.793, 6.686 and 16.045 for PC1–3,
respectively; all at P<0.001). Along PC1, raking separated from
chewing (P<0.001) but not from strikes (P=0.762), driven
by an earlier time to peak in all kinematic displacements
(Fig. 6). Increased amplitude
of hyoid, mandibular and pectoral girdle motion separated raking from chewing
(P<0.05) but not from strikes (P=0.053) along PC2, while
increased cranial elevation drove raking from other behaviors
(P<0.001) and chewing from strikes (P<0.05) along PC3
(Fig. 6). Raking thus differed
significantly from at least one of the other behaviors along all informative
PC axes.
|
Raking biomechanical models
In both taxa, the raking preparatory phase involves two musculoskeletal
events. Concomitant mandibular jaw occlusion and basihyal protraction
immobilizes the prey between the mandibular and TBA jaws
(Fig. 2) and effectively
`charges' the TBA for the power stroke
(Fig. 7A,B). Mandibular jaw
occlusion is rigorously maintained throughout the rake, and, after the
preparatory phase, the raking power stroke may be accomplished by a
combination of the following biomechanical mechanisms, which are discussed in
detail below (see also Movie 3 in supplementary material): (1) anterodorsally
directed rotation of the dorsal TBA jaw via cranial elevation
(Fig. 7C,D); (2) posterior
excursion of the basihyal via two complementary musculoskeletal
pathways – (a) indirectly via hypaxialis-driven pectoral girdle
retraction (Fig. 7E,F) and (b)
directly, via sternohyoideus contraction
(Fig. 7G,H).
|
|
DISCUSSION |
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|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
; Ishiguro et al.,
2003). Below, we synthesize the interspecific similarities and
differences in TBA morphology and raking kinematics with available muscle
activity evidence (Konow and Sanford,
2008) and discuss the implications to our biomechanical hypotheses
for TBA function during raking.
Clear similarities in TBA gross morphology existed in O. mykiss
and S. jardinii, including the presence of (1) basihyal dentition,
(2) opposing dentition in the oral cavity roof and (3) a cleithrobranchial
ligament (CBL). Dentition on various bone surfaces inside the oral and
anterior buccal cavity is a basal trait in teleosts
(Hilton, 2001). Thus, the
convergent evolution of a CBL and associated hypertrophy of basihyal and
opposing mouth roof dentition appears to be an example of an `evolutionarily
stable configuration' (Schwenk and Wagner,
2000; Wagner and Schwenk,
2000). Despite the convergent TBA morphology, these traits
differed qualitatively between taxa, in (1) TBA upper jaw dentition
distribution, (2) dentition morphology in the TBA jaws and (3) different
origin-insertion paths of the CBL. This supports earlier notions that the TBA
is a character suite and not a single trait
(Hilton, 2001), and the
morphological differences emphasize that TBAs are not unambiguous
inter-lineage convergent traits (Sanford,
2001b).
Strongly convergent trends were also evident in raking kinematics,
including a gross behavioral sequencing into distinct, successive compressive
preparatory, excursive power-stroke and expansive recovery phases
(Sanford, 2001b). Raking
kinematics involved concomitant cranial elevation and pectoral girdle
retraction during the power stroke in both taxa, which is also a ubiquitous
suction-feeding characteristic. During raking, pectoral girdle retraction is
notably amplified compared with other feeding behaviors and is coupled with a
novel preparatory hyoid protraction and early jaw occlusion, maintained to
different extents in each taxon throughout the power stroke. Therefore, rather
than resulting from entirely novel skull kinematics, our results suggest that
raking is governed by a combination of derived kinematics (amplified pectoral
girdle retraction, hyoid protraction followed by retraction). Meanwhile, the
convergent changes in timing of the mandible, cranium and pectoral girdle
motion during raking are relatively slight modifications of more basal aquatic
behaviors, such as ventilation (Liem,
1984; Liem, 1985),
prey capture (Lauder, 1985;
Carroll, 2004) and
prey-processing (Sibbing,
1982). Sampling of one taxon representative from each lineage is
not conclusive evidence that raking between all the members of each lineage is
convergent. Nevertheless, based on the morphology of the TBA among other
representatives of these two lineages
(Konow et al., 2008) and
previous kinematic evidence (Sanford,
2001a; Sanford,
2001b), we propose a biomechanical model to be used to
quantitatively evaluate the level of raking convergence between multiple taxa
from each lineage.
The input kinematic excursions in O. mykiss (neurocranial
elevation, 22.41±1.23 deg.; pectoral girdle retraction,
0.75±0.06 cm) were less pronounced than in Salvelinus
fontinalis (38.6±1.1 deg.; 0.83±0.06 cm), the only salmonid
for which raking kinematics were previously presented
(Sanford, 2001b;
Konow et al., 2008). Moreover,
S. jardinii displayed reduced neurocranial elevation
(13.05±1.01 deg.) and amplified pectoral girdle retraction
(0.41±0.13 cm) compared with Osteoglossum bichirrosum (ne: 26,
27±1.6 deg.; pg: 0.22±0.02 cm), an osteoglossid sister taxon
(Sanford and Lauder, 1990),
but much less neurocranial elevation than in the notopterid Xenomystus
nigri (34.7±1.03 deg.)
(Sanford, 2001a). Thus, raking
kinematics in the study taxa presented here were not as similar as predicted,
based on evidence from their close sister taxa, corroborating Sanford's
finding that considerable kinematic differences can exist in raking kinematics
(Sanford, 2001a) despite close
phylogenetic position and similar TBA morphology
(Taverne, 1979). This further
suggests that even subtle differences in muscle activity and recruitment can
result in functionally divergent raking kinematics
(Sanford, 2001a). An
interesting future avenue of research would be to compare the relative
magnitude of contribution from neurocranial and pectoral girdle input
kinematics to basihyal output kinematics during the power stroke.
Our results suggest that, although raking behaviors are generally driven by
the same input kinematics in both lineages, subtle interspecific differences
are also present, namely in the magnitude of cranial elevation and pectoral
girdle kinesis. Meanwhile, timing variables are less influential on taxon
segregation, which may indicate that (1) raking is governed by tight
neuro-motor control, suggesting temporal stereotypy (e.g.
Alfaro et al., 2001;
Ross et al., 2007), and (2)
behavioral modulation, and not interspecific differences in one or both taxa,
results in the observed differences in power-stroke excursion magnitudes
(Konow et al., 2008).
The more variable raking kinematics in S. jardinii compared with
O. mykiss (Fig. 5)
correspond well with muscle activity differences between these taxa, involving
convergence of AM and m. protractor hyoideus (PH) activity during the
preparatory phase and diversity in SH, m. hypaxialis (HP) and m. epaxialis
activity during the power-stroke phase [see
fig. 5 in Konow and Sanford
(Konow and Sanford, 2008)].
Thus, while raking relies on a convergently derived shift in musculoskeletal
function, subsequent diversification in raking kinematics may have occurred
(Sanford and Lauder, 1990;
Sanford, 2001a).
For example, our data suggest that osteoglossid raking kinematics is more
complex than a previous analysis of Osteoglossum bicirrhosum revealed
(Sanford and Lauder, 1990).
Notable cranial depression and subtle pectoral girdle protraction occur during
the raking preparatory phase in S. jardinii, presumably augmenting
basihyal protraction relative to the TBA upper jaw. This preparatory
protraction increases the distance that the basihyal moves when retracted
during the power stroke, an augmented TBA `priming' that may explain the
restricted cranial elevation and pectoral girdle retraction in S.
jardinii compared with O. mykiss, which does not display such
extensive preparatory kinesis. Moreover, pronounced hyoid elevation and firmer
mandibular jaw occlusion in S. jardinii suggest that compressive
forces onto the prey are achieved, which may reduce the need for the extensive
neurocranial and pectoral girdle power-stroke excursions commonly seen in
other raking taxa (Lauder and Liem,
1983; Sanford and Lauder,
1989).
Compressive raking kinematics in S. jardinii may interplay with
morphological specializations, which involve a rigid oral cavity roof with a
chevron-shaped cross section and a lateral profile that is anterodorsally
inclining [see also fig. 2 in
Sanford and Lauder (Sanford and Lauder,
1990)]. The millstone-like TBA tooth plates are thus angled at 45
deg. relative to the body axis in S. jardinii whereas the tooth
plates in O. mykiss are parallel to the body axis
(Fig. 3). Differences in CBL
morphology may be a key component in altering the transmission efficiency of
hypaxial strain into basihyal power-stroke kinesis. A straight CBL may
theoretically deliver a more direct and rapid hypaxial strain transmission in
S. jardinii. An arc-shaped ligament, on the other hand, may explain
the faster and amplified cranial and pectoral girdle kinematics in O.
mykiss, which act to straighten the CBL in order to achieve powerful
posteriorly directed basihyal raking motion. Alternatively, amplified
power-stroke kinematics may not only serve to reduce hard prey but also to
immobilize more elusive naturally selected prey, a function that future
studies of modulation in response to different prey types may answer
(Sanford, 2001b;
Konow et al., 2008).
Intra-pectoral flexion, via articulations between the coracoid,
cleithral, supracleithral and postcleithral girdle elements, is another
potentially important and hitherto unexamined variable. Specimen manipulations
revealed inter-specific differences in intra-pectoral flexion, which in both
study taxa exceeded values for taxa presented by Muller
(Muller, 1987). Associated
kinematic differences, if present, remain unquantified, as the pectoral girdle
is largely obscured by the operculum in live specimens. However, high-speed
videos of one S. jardinii specimen with eroded operculi have revealed
that there is some rotational movement between the posttemporal and
supracleithrum, which may be facilitated by epaxial regional specialization
(Thys, 1997;
Carroll, 2004). Basal teleosts
lack a protractor pectoralis (Greenwood
and Lauder, 1981), yet the fiber orientation of other deep
muscles, e.g. the obliquus superioris, pharyngocleithrals internus or p.
externus, may permit such complex pectoral girdle kinesis [see
fig. 7 in Lauder and Liem
(Lauder and Liem, 1980)].
Is raking a convergently derived behavior?
Quantitative comparisons of raking in the representative ingroups
(osteoglossomorphs and salmonids) with other behaviors existing in both
ingroups and outgroups (Esox and Amia) provide strong
support for the hypothesis that raking is convergently derived in the two
TBA-bearing lineages. Coupled with the changes in morphology discussed above,
raking results from a convergently derived shift in the muscle activity
pattern; specifically, an early onset occurs in hyoid protractor and
mandibular adductor muscles (Konow and
Sanford, 2008). This novel MAP yields the differences in phase
sequencing between the examined feeding behaviors
(Table 1B). Our results also
suggest that rakes differed more from chews than strikes and, indeed, raking
could be a functional derivative of a `closed-mouth strike'. Raking also
differed from both chews and strikes by having a more pronounced pectoral
girdle kinesis and from strikes by gape closing and hyoid elevation movement
during the power strokes of the respective behaviors. During raking there is
extensive pectoral girdle retraction, and the limited dorsoventral movement of
the basihyal suggests that it is moving primarily anteroposteriorly during the
power stroke. Sonomicrometry data from other taxa, including raking taxa,
suggest that basihyal output kinematics may be partly obscured using external
landmarks (Sanford and Wainwright,
2002; Konow et al.,
2008). However, it is clear from the present study that the
derived variables all loaded heavily along statistically informative PC axes
and described three input kinematic mechanisms for modeling of the raking
power stroke.
TBA biomechanical models
The musculoskeletal configuration of the TBA and the temporal sequence of
raking indicate that this system primarily functions in an anteroposterior
direction in the midsagittal plane, as confirmed in ventral view. Moreover,
the externally visible kinematics of the mandible, neurocranium and pectoral
girdle suggests that the input mechanisms function synergistically. Using the
data presented herein, and based on modifications to existing four-bar linkage
and third-order lever models (Muller,
1987; Carroll,
2004; van Wassenbergh et al.,
2005), we propose three complementary and synergistic component
models for raking biomechanics (Fig.
7). The models will aid future quantifications of the relative
contribution of each to the overall raking pattern both within and between
taxa (Wainwright et al., 2004;
Grubich and Westneat, 2006).
Future multi-taxon analyses may empirically calibrate the models and determine
if these input mechanisms synergistically result in functional many-to-one
mapping (Alfaro et al.,
2005).
Component models
As outlined above, the raking preparatory phase involves protraction of the
basihyal and occlusion of the mandibular jaws
(Fig. 7A,B). The role of
cranial elevation during the subsequent raking power stroke differs from its
role during, for example, strikes (Fig.
7C,D), while still functioning as a third-order lever
(Carroll, 2004;
Carroll and Wainwright, 2006).
During strikes, epaxial shortening causes cranial elevation, which drives
inter-opercular rotation, maxillary rotation, jaw protrusion and/or hyoid
depression (Anker, 1974;
Motta, 1984;
Muller, 1987;
Muller, 1989;
Westneat, 1991). However,
since all these output kinematics during raking are impeded by jaw occlusion,
cranial elevation instead causes anterior displacement of the TBA upper jaw
from the posteriorly moving lower (basihyal) jaw
(Fig. 7E,F).
During the raking power stroke, TBA gape distance is maintained relatively
constant, as indicated by the 0.1–0.2 cm dorsoventral hyoid
excursion measured in both taxa. Mandibular jaw motion was also relatively
restricted in both taxa (0.1 cm in S. jardinii; 0.2 cm in O.
mykiss) and did not contribute statistically to taxon separation.
Dorsoventral compression of the TBA is augmented throughout the power stroke
by maintained mandibular jaw occlusion in both taxa. Moreover, the prolonged
PH contraction in S. jardinii further impedes posteriorly directed
hyoid excursion (Konow and Sanford,
2008). While pronounced variation exists in other raking input
kinematics, occluded mandibular jaws during the raking power stroke appear to
be a ubiquitous trait (Sanford and Lauder,
1989; Sanford and Lauder,
1990; Sanford,
2001a). Thus, dorsoventral TBA compression may contribute to an
efficient raking power stroke.
We model hypaxial strain transmission during the raking power stroke,
via the pectoral girdle and sternohyoideus–cleithrobranchial
ligament (SH–CBL) complex to basihyal retraction, using a four-bar
planar linkage model (Fig.
7E,F). The model builds on the four-bar links in Muller's hyoid
depression model (Muller,
1987); however, in our model, the `fixed link' is the distance
from the interhyal–symplectic joint, via the hyomandible and
neurocranium, to the posttemporal–supracleithral joint (i.e. Muller's
input link). At this joint, the pectoral girdle `input link' (Muller's fixed
link) articulates with the neurocranium. The `coupler link' extends from the
CBL origin on the ventromedial pectoral girdle, via the SH–CBL
complex, to the ceratohyal–basihyal joint (Muller's output link), from
where the anterior and posterior ceratohyal `output link' connects,
via a short and stout interhyal, onto the suspensorium (Muller's
coupler link).
Uncertainties regarding the validity of the proposed model as well as existing four-bar linkage models (including Muller's model) are addressed in detail below.
). ;
van Wassenbergh et al., 2007;
Carroll, 2004). Isotonic
contraction of the SH during raking will cause posteriorly directed basihyal
retraction (Fig. 7G,H), while
eccentric or absent SH contraction during HP-mediated pectoral girdle
retraction will cause SH stretching, which in the case of O. mykiss
will straighten the arc-shaped CBL. Sonomicrometry measurements from O.
mykiss have shown that maximal SH stretching is restricted to approx 2%
of SH resting length, a limitation that likely is explained by straightening
of the arc-shaped CBL (Konow and Sanford,
2008). The PH mechanically antagonizes the basihyal retractor
musculature (SH and HP). During the raking preparatory phase, we propose that
PH shortening protracts the basihyal towards the mandibular symphysis, thereby
maximizing the subsequent basihyal retraction during the power stroke. A
maintained PH contraction during the power stroke, as observed in S.
jardinii, mechanically prevents basihyal retraction, from which
coupler-link stretching and basihyal elevation may result
(Konow and Sanford, 2008).
Moreover, maximal lower jaw depression, coupled with hyoid depression during
strikes, may also result in straightening of the arc-shaped salmonid CBL,
which only when straightened will be capable of direct force transmission from
hypaxial musculature to the basihyal, functionally decoupling the SH. While
the coupler link (Muller's output link) clearly is one of the more `irregular'
four-bar links, it is uniquely reinforced by a CBL in all raking teleosts
(although absent in Pantodon)
(Sanford and Lauder, 1990).
The coupler link distortion that could result from the musculoskeletal
dynamics in the ventral TBA may be at least partly mitigated by the presence
of a straight CBL in osteoglossomorphs
(Sanford and Lauder, 1989;
Hilton, 2001;
Konow and Sanford, 2008).
This, however, assumes that the CBL is not an elastic structure, which is
currently under investigation. ), a pattern that
has already been quantified via sonomicrometry
(Sanford and Wainwright,
2002). However, this link describes both dorsoventrally
curvilinear basihyal motion during strikes and chews and anteroposterior
ellipsoid motion during rakes. Although flaring of the suspensorium means that
the four-bar output link deviates from 2-D, some of this motion is absorbed by
interhyal rotation, which permits the hyoid bar to initially shift
posteriorly, like during suction feeding
(De Visser and Barel, 1996).
Flaring clearly diverges from the 2-D motions that can be explained by
conventional engineering four-bar linkage theory. However, the discrepancies
in output link length required to alter basihyal motion from curvilinear
(Sanford and Wainwright, 2002)
to ellipsoid are theoretically restricted to the freedom of motion around the
interhyal, which connects the ceratohyal output link to the suspensorial fixed
link (De Visser and Barel,
1996; Muller,
1996).
Testing and calibrating the four-bar model
The functional deviations from planar four-bar linkage theory outlined
above are far from unprecedented examples of how four-bar models inaccurately
quantify musculoskeletal systems. Nevertheless, four-bar models retain their
usefulness by reducing organismal complexity to a level that is
computationally more feasible and permits calculation of lever ratios and
mechanical advantages [viz. Fig.
3 vs Fig. 7A and
7E,F; illustrating that the hyoid linkage proposed herein, and by
Muller (Muller, 1987), in
organismal reality is a `10-bar']. Interspecific differences were seen in all
kinematic input mechanisms driving raking power strokes. Consequently, the
model hypotheses presented herein will be important contributions in future
comparative studies of raking, both within and between the phylogenetically
unrelated raking lineages and across the organizational levels of morphology,
muscle activity and kinematics (Muller,
1987). Detection of, and compensation for, link distortion or link
2-D deviations is possible using sonomicrometry
(Sanford and Wainwright, 2002)
or 3-D fluoroscopy (Brainerd et al.,
2007), which may provide taxon-specific empirical data to
calibrate the raking four-bar linkage. Currently, direct tests of
biomechanical models in aquatic vertebrate feeding remain limited to
volumetric expansion during suction feeding
(Muller and Osse, 1984;
Van Wassenbergh et al., 2006),
sonomicrometric quantifications of hyoid depression in suction feeding
(Sanford and Wainwright, 2002;
Wilga and Sanford, 2008) and
the effect of cranial elevation on suction-pressure generation
(Carroll, 2004;
Carroll and Wainwright, 2006).
Few complete four-bar linkage models have undergone comprehensive empirical
testing (van Wassenbergh et al.,
2005; Roos et al.,
2008), yet component links have been dynamically quantified
[viz. the levator posterior muscle in a four-bar model of Grubich and
Westneat (Grubich and Westneat,
2006)].
Basal and derived raking mechanisms
Basihyal elevation and protraction during the preparatory phase, combined
with a power stroke driven by cranial elevation, is a conservative combination
of raking input mechanisms in salmonids
(Sanford, 2001b) (present
study). This pattern also occurs in some osteoglossomorphs
[Osteoglossum (Sanford and
Lauder, 1990); Xenomystus
(Sanford, 2001a)], while other
taxa mainly utilize pectoral girdle retraction
(Sanford and Lauder, 1989).
Analyses of Hiodon, the basal-most osteoglossomorph and extant raking
taxon (Hilton, 2003;
Lavoué and Sullivan,
2004), may confirm the ancestral input mechanisms. This would help
determine whether salmonids use a basal or derived suite of input mechanisms
and permit quantification of the evolutionary changes in input mechanisms
within and among the raking lineages. Phylogenetic hypotheses and fossils are
plentiful for both lineages and their relatives
(Stiassny et al., 1996;
Ishiguro et al., 2003).
Time-calibrated analyses could thus yield robust tests of how different
component mechanisms contribute to functional disparity. Such analyses would
significantly improve our understanding of how evolutionary rates in the
evolution of structural and functional disparity influence the differentiation
of novel behaviors.
LIST OF SYMBOLS AND ABBREVIATIONS
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Acknowledgments |
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Footnotes |
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|
References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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