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First published online January 17, 2007
Journal of Experimental Biology 210, 495-504 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02663
Biting releases constraints on moray eel feeding kinematics
Section of Evolution and Ecology, University of California, One Shields Avenue, Davis, CA 95616, USA
* Author for correspondence (e-mail: rsmehta{at}ucdavis.edu)
Accepted 22 November 2006
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Key words: moray eel, feeding, anatomical reduction, kinematic integration, Muraena retifera, Echidna nebulosa, Amphilophus citrinellus, Lepomis macrochirus, Micropterus salmoides
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; Lauder,
1985; Liem, 1980;
Van Leeuwen, 1984), a fact
that has been partly attributed to the demands of feeding in a medium much
more viscous and dense than air (Lauder,
1985). However, several fish groups have developed around
alternative feeding strategies, including parrotfishes (Scaridae),
surgeonfishes (Acanthuridae), gar (Lepisosteidae) and, as we argue in this
paper, moray eels (Muraenidae). In each of these groups prey are captured by
direct biting, although subsequent transport behaviors may involve hydraulic,
suction-based mechanisms (e.g. Lauder,
1983), and comparative research with these groups has provided
some insights into how suction feeding shapes and constrains patterns of
muscle activity and movement (Alfaro et
al., 2001; Lauder,
1980a; Lauder,
1980b; Lauder and Norton,
1980; Porter and Motta,
2004). Because capturing prey by biting and suction rely on
different mechanical events (e.g. cranial adduction vs abduction,
forceful contact of the teeth with the prey vs the generation of
fluid flow), there may be general differences in the functional patterns that
are associated with these behaviors. Biting and suction may be associated with
different morphological specializations of the skull that reflect different
mechanical demands (De Visser and Barel,
1998; Wainwright and Bellwood,
2002), and this may have implications for kinematics and motor
patterns (Alfaro et al., 2001;
Rice and Westneat, 2005). In a
phylogenetically broad comparative analysis
(Alfaro et al., 2001), several
features of the muscle activity pattern differed consistently between biting
and suction prey capture, including a briefer latency between the activation
of expansion and compression phase muscles during suction feeding.
Suction-feeding behavior may also generally be quicker than prey capture by
biting. Fishes that rely on high-velocity lunges followed by biting, rather
than suction, exhibit longer strike times
(Porter and Motta, 2004), and
the kinematics of benthic biters appears to typically be slower than suction
feeding (Alfaro et al., 2001;
Rice and Westneat, 2005;
Konow and Bellwood, 2005).
Successful suction feeding is thought to depend on the ability to generate
high water flow velocities, by rapidly expanding the mouth and buccal cavity
(Van Leeuwen and Muller, 1984;
Wainwright et al., 2001;
Van Wassenbergh et al., 2006).
A set of inter-related linkage systems
(Anker, 1974;
Muller, 1989;
Westneat, 1994) creates a
posterior wave of oral expansion that results in both water and prey being
drawn into the buccal cavity. The rate of buccal expansion is directly related
to peak fluid speed magnitude (Day et al.,
2005), suggesting that the speed of cranial movements of suction
feeders during the earliest stages of prey capture can influence their
success. Mouth opening speed or peak gape may not affect predatory success in
biters as prey capture occurs during jaw adduction after peak gape, rather
than during buccal expansion, as in suction feeders. These differences in the
timing of coordinated cranial movements during prey capture suggest that the
kinematics of successful suction feeding may be constrained, in comparison to
biting, such that suction feeders exhibit relatively low variance and tight
integration in movement patterns during the period of the strike leading up to
prey capture. However, this possibility has not yet been explored in
comparative studies of aquatic feeding vertebrates.
Anguilliform eels of the family Muraenidae are a substantial radiation of
about 185 species of predatory fishes that mostly live in coral reefs of warm
and temperate marine waters (Nelson,
2006; Böhlke et al.,
1989). Like all anguilliforms, morays lack pelvic fins, but in
addition all muraenids lack a pectoral fin and show a highly reduced pectoral
girdle (Böhlke et al.,
1989; Fielitz,
2002; Gregory,
1933). In this paper we explore this and other exceptional
anatomical features of the moray skull and ask what consequences they have for
feeding function. We test for the presence of suction feeding in two moray
species by measuring the extent to which prey are transported toward the mouth
of striking eels. Skull kinematics and suction ability in the two morays are
compared to Anguilla rostrata, an anguillid eel that possesses a
well-developed pectoral fin and pectoral girdle. We conclude that morays do
not use suction during prey capture and we go on to examine the effects that
the alternative prey capture strategy, biting, has on moray feeding
kinematics. In particular, we test the hypothesis that the absence of suction
feeding in morays has reduced constraints on kinematic integration, permitting
them to show greater variance in traits that characterize the timing and
extent of motion of the skull and jaws. To test the above hypothesis, we
compare the feeding kinematics of the two moray eel species to a
phylogenetically wide sample of suction feeders, including Anguilla
rostrata, two centrarchid species well known for being strong suction
feeders, and a Central American cichlid.
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;
Yukihira et al., 1994). Prey
capture morphology and kinematics of the morays were initially compared to
those of the anguillid eel Anguilla rostrata (Lesueur). A.
rostrata feeds on a diversity of larval insects as well as gastropods,
oligochaetes, amphipods and fish (Page and
Burr, 1991). In order to test for the effect of suction feeding on
the variability of skull movement during prey capture the two moray eel
species were compared to Anguilla rostrata and three perciform
species: the North American centrarchids, Lepomis macrochirus
(Rafinesque) and Micropterus salmoides (Lacépède), and
the Central American cichlid, Amphilophus citrinellus (Günther).
Both L. macrochirus and M. salmoides have been the focus of
many studies related to suction feeding, and these species are known to differ
in their ability to produce suction
(Carroll et al., 2004;
Higham et al., 2005;
Higham et al., 2006a;
Higham et al., 2006b;
Wainwright and Shaw, 1999).
Like the two centrarchids, Amphilophus citrinellus is known to use a
combination of ram and suction during prey capture
(Higham et al., 2006b). We
used Centrarchids and Cichlids, percomorph fish that are strong suction
feeders and are phylogenetically distant from the anguilliforms, because they
provided a robust test of the prediction that there would be differences
between biting and suction-feeding taxa in the variability of feeding
kinematics.
The M. retifera (standard lengths SL = 35.5 and 40.3 cm)
were collected in the Florida Keys, E. nebulosa (SL = 17.3,
19.5, 28.5 and 35.5 cm) were collected in Hawaii and obtained commercially,
A. rostrata (SL = 58.2 and 63.6 cm) were collected in Woods
Hole, MA, USA, L. macrochirus (SL = 15, 15 and 16 cm) and
M. salmoides (SL = 16.6, 17.3 and 18.4 cm) were collected
locally in Yolo County, CA, USA, and the A. citrinellus (SL
= 8.6, 9.6 and 11.5 cm) were obtained commercially from a pet dealer. At
the conclusion of the experiments, all of the specimens were dissected, either
while fresh or following formalin fixation, and at least one specimen of each
species was cleared and stained for bone and cartilage following a
modification of Dingerkus and Uhler
(Dingerkus and Uhler,
1977).
Individuals were housed and filmed at 22–27°C in 100 l aquaria at the University of California, Davis using a NAC Memrecam ci digital system (Tokyo, Japan) with illumination from two 600 W flood lights. Video sequences of A. rostrata, L. macrochirus, M. salmoides and A. citrinellus were recorded at 500 images s–1, and sequences of the moray eels were recorded at 100 images s–1. Distances in the images were scaled by recording an image of a ruler placed in the field of view. All fish were filmed feeding on pieces of cut squid (Loligo sp.).
To quantify feeding kinematics, we analyzed images from the video sequences with the aid of Scion Image software. Due to the diverse cranial morphology of the species in this study, we analyzed only kinematic variables that could be considered homologous across the six taxa. We measured the x, y coordinates of six landmarks from the images: (i) the anterior tip of the premaxilla (upper jaw), (ii) quadrate-articular jaw joint, (iii) anterior tip of dentary (lower jaw), (iv) neurocranium-vertebral joint (v) anteriormost margin of the orbit (reference point on the neurocranium), (vi) ventral-most point of the orbit, (vii) ventral-most extension of the floor of the mouth (perpendicular distance between a line at the ventral-most point of the orbit), and (viii) center of mass of the prey. Coordinates of these landmarks were measured at five points in time: (i) onset of the strike characterized by the onset of fast lower jaw rotation, (ii) time of peak jaw abduction, (iii) time of peak cranial elevation, time of peak gape, (iv) peak hyoid displacement, and (v) time of prey capture, defined as the frame in which the prey completely entered the predator's mouth or, in eels, the frame in which the upper and lower jaws made contact with the prey.
As an indication of the use of suction in prey capture we measured `suction
distance', the distance the prey moved toward the plane of the open mouth
during the strike. Suction distance has been used extensively as a functional
measure of the contribution of suction-induced flow to the movement of prey
into the oral cavity (Norton and Brainerd,
1993; Svanbäck et al.,
2002; Wainwright et al.,
2001). While the absence of suction distance does not necessarily
imply the inability to generate suction pressures inside the buccal cavity,
greater suction distances do imply stronger suction pressures for an
individual fish (Van Wassenbergh et al.,
2006; Wainwright et al.,
2001). Thus, from each prey capture sequence, we determined the
rotational excursions of the lower jaw and the neurocranium, peak hyoid
depression and gape distance, and the time from the onset of jaw depression to
peak jaw rotation, peak cranial rotation, peak hyoid depression and prey
capture. In addition, we counted the number of times the direction of head and
jaw excursion was temporarily reversed in the time between the onset of jaw
depression and the time of peak jaw and head rotation, respectively. We
analyzed only those sequences in which a lateral view of the fish could
clearly be seen in the image and the head of the fish was oriented
approximately perpendicular to the camera. A total of 169 prey capture
sequences were analyzed in this study, with sample sizes ranging between
9–10 for each individual.
We used a nested analysis of variance (ANOVA), with individuals nested within species to compare the average value for each kinematic variable between moray eels and A. rostrata. Kinematic data were log10 transformed before analyses to help normalize variances. We used a sequential Bonferroni correction to adjust the probability values for the use of multiple statistical tests. Prior to running the nested ANOVAs, data were inspected for normality and Levene's tests were performed to assess equality of variances. Although ANOVA is generally robust to some departures from the assumption of equal variances, we also performed Kruskal–Wallis non-parametric comparisons on average kinematic variables.
To identify independent axes of kinematic variation between moray eels and
A. rostrata, we conducted a principal component analysis (PCA) on the
correlation matrix of a reduced set of variables from the entire data set. In
this analysis we included jaw rotation, head rotation, the number of reversals
of jaw rotation and head rotation, time to peak jaw rotation, time to peak
head rotation, time to peak gape, and time to prey capture. Predator size has
been shown to have strong effects on feeding kinematics and is therefore a
potentially confounding factor. For suction-feeding fish, scaling effects are
most acute for duration variables such as time to peak gape and peak hyoid
displacement (Richard and Wainwright,
1995; Van Wassenbergh et al.,
2005). We tested for body size effects in the data set by
regressing principal component scores against the logarithm of fish body mass
(Mb).
In order to test for differences among all six species in the variability of prey capture kinematics, we ran a nested ANOVA on kinematic variance calculated for each individual fish. Kinematic variance was calculated for each fish by summing the variances for scores on each of the first four principal component axes (these PCs had eigenvalues greater than 1.0) of a PCA that was conducted on the kinematic data set for all six species. A nested ANOVA was then run on kinematic variance with species nested within group, where the two groups were moray eels (non-suction feeders) and the suction feeders. A significant test of the group effect in this ANOVA would indicate that the variance of prey capture kinematics differs between the morays and the four suction-feeding teleosts. We used SYSTAT version 9 (SPSS Inc., Chicago, IL, USA) for all statistical analyses.
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;
Nelson, 2006). In accordance
with Fielitz (Fielitz, 2002),
we found the pectoral girdle to be greatly reduced with only one pectoral bony
element present in both E. nebulosa and M. retifera. Ventral
elements of the hyoid arch and the three gill-bearing branchial arches are
greatly reduced in size. The hyoid is long, thin (0.11–0.4 mm in their
thickest dimension in our specimens), and flexible
(Fig. 1B,D). The
sternohyoideus, which attaches anteriorly to the hyoid arch, is represented by
ventrolateral extensions of the hypaxial musculature. The sternohyoideus
muscle is small compared to other teleosts and the fibers appear continuous
with the hypaxialis.
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In Anguilla rostrata, the premaxillae of the upper jaw is fused with the ethmovomer complex and is immobile (Fig. 1E). The maxillae attach to the neurocranium just posterior to the premaxillae via the premaxillae-ethmovomer complex and is slightly mobile. The premaxillae, maxillae and mandible bear very small sharp teeth arranged in many rows. There is also a narrow patch of very small sharp densely packed teeth on the vomer. The suspensorium is narrow. The pterygoid is well-developed and the hyomandibula and quadrate are directed anteriorly so the lower jaw is more compact. The opercular series is well developed and the opercles are large and crescent-shaped. The hyoid complex is long and robust. The basihyal is elongate while the urohyal and ceratohyals are thick (Fig. 1F). A well-developed sternohyoideus muscle originates on a robust pectoral girdle and attaches anteriorly to the hyoid arch.
All eels initiated the strike with lower jaw depression, accompanied by cranial elevation. Neither of the two moray species exhibited any hyoid depression during the strike and prey did not enter the oral jaws until some time after peak gape (Figs 2, 3 and 4). The kinematics of prey capture for A. rostrata followed a familiar pattern of events, which included hyoid depression (Figs 2 and 3). In fact, A. rostrata synchronized lower jaw depression and cranial elevation with depression of the hyoid, which reached maximum a few milliseconds after peak jaw rotation, a pattern observed in suction-feeding perciforms (Table 1; Fig. 3). As with other suction feeders, prey entered the oral cavity of A. rostrata near the time of peak gape.
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Although the order of kinematic events was similar in morays and the anguillid eel, all average magnitudes and timing events for kinematic variables were significantly different between morays and A. rostrata (Table 1). Jaw rotation in morays was nearly three times that of A. rostrata, which exhibited very small angular excursions of the lower jaw. Head rotation was also four times greater in morays compared to A. rostrata, which exhibited modest head excursions ranging from 1.19–6.34°. Over all, morays exhibited significantly slower skull movements during prey capture compared to A. rostrata (Figs 2, 3 and 4).
Morays interrupted the expansion phase of the strike with temporary reversals of both jaw and head rotation that occurred at any point between the onset of jaw depression and the moment of prey capture. In some trials both the lower jaw and neurocranium reversed directions (e.g. Fig. 4) whereas in other trials, only one morphological unit (jaw or neurocranium) would reverse direction. Head reversals were slightly more frequent than jaw reversals. The number of reversals was not correlated with strike initiation distance (r2=0.01). Reversals of jaw or head rotation were never seen in A. rostrata and have yet to be documented in any suction-feeding species.
Anguilla rostrata used considerable suction during prey capture, as indicated by suction distances between 10–13 mm in front of the mouth aperture (Table 1). These suction distances corresponded to a range of 44–71% of peak gape distance. In contrast, there was no evidence of prey moving toward the mouth of either moray species in any of the video sequences, indicating no use of suction to transport prey during capture.
The first principal component revealed complete separation in kinematic space between the morays and A. rostrata, with morays having higher scores on this axis (Fig. 5). All of the angular excursions and timing variables loaded heavily and positively on PC1 (68%) while the kinematic reversals loaded strongly on PC2 (Table 2). PC1 reflected the longer times in the moray feeding sequences, which were more spread out, reflecting greater variability. The second axis of variation, PC2 (17%), loaded heavily on the number of angular reversals, which also varied between moray feeding sequences. There was no relationship between body mass on either of the PC axes: PC1 (r2<0.02, F1,8=0.21, P=0.76) or PC2 (r2<0.010, F1,8=0.32, P=0.69). Thus, these principle components identified size-independent patterns of variation among the three anguilliform taxa.
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Time to prey capture in A. rostrata, the two centrarchids and the cichlid ranged from 16–70 ms from the onset of jaw depression, while the two moray species ranged from 189–1186 ms. A regression analysis indicated that there was no relationship between body mass and average prey capture time for all fish (r2=0.02, F1,15=0.35, P=0.56). A nested ANOVA comparing averages of the kinematic variables in morays to the four suction-feeding species indicated significant differences in all kinematic variables, with the exception of cranial elevation (Table 1). However, cranial elevation showed significant differences in variance across the two groups in the Levene's test. Kuskal–Wallis non-parametric tests showed differences in all six kinematic variables between morays and the other four species (all P<0.001).
A nested ANOVA with individual nested within group (morays vs suction feeders), indicated that the variance in feeding kinematics differed in the two groups (F1,3=60.11, P<0.005). Summed variance on the first four principal components was about 5 times higher for the morays, averaging 4.42 per species as compared to 0.837 for the suction feeders (Table 1).
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;
Lauder, 1985;
De Visser and Barel, 1998;
Sanford and Wainwright, 2002).
The apparent reduction in suction-feeding ability was supported by the
analyses of prey capture kinematics that revealed no hyoid depression and no
movement of prey toward the eel's mouth in the 59 moray feeding sequences
collected in this study (Table
1). E. nebulosa and M. retifera did not use
suction-induced water flow to help close the distance between them and their
prey, but rather, apprehended their prey by direct biting.
Biting is associated with several novel features in the prey capture
kinematics of morays. Although the basic kinematic sequence of jaw depression
and cranial elevation did not differ from that seen in a representative
suction-feeding eel, Anguilla rostrata, and was similar to both
centrachids and A. citrinellus, cranial movements were distinguished
by being significantly slower and more variable. Relatively slow movements
have been found in other teleost taxa that apprehend their prey by biting. For
example, time to maximum gape or peak lower jaw depression takes over 200 ms
in the wimple piranha (Janovetz,
2005), about 150 ms in the redfin needlefish
(Porter and Motta, 2004), over
300 ms in the koran angelfish (Konow and
Bellwood, 2005), and about 80 ms in the bucktooth parrotfish
(Rice and Westneat, 2005).
Effective suction feeding involves a rapid and coordinated
anterior-to-posterior expansion of the mouth, buccal and opercular cavities
(Lauder, 1980a;
Lauder, 1985;
Svanbäck et al., 2002).
The velocity of water flow that is generated, and hence the speed with which a
prey item is transported to the mouth, is directly dependent on the rate of
expansion of the buccal cavity (Muller et
al., 1982; Van Wassenbergh et
al., 2006). Prey capture and time to peak gape expansion in
suction-feeding teleosts typically occur in less than 60 ms from the onset of
mouth opening (Gibb and Ferry-Graham,
2005; Lauder,
1985; Wainwright et al.,
2001) and occurred in less than 50 ms in the species studied here.
In contrast, morays captured prey in about 500 ms, approximately an order of
magnitude longer in time than seen in A. rostrata, the two
centrarchids and the cichlid. We have been unable to find any examples of
similar sized suction-feeding teleosts in the literature with strike times as
long as 500 ms.
The suction feeders examined in this study captured their prey by depressing the hyoid apparatus and expanding the oral cavity, thus manipulating the water around the prey, whereas moray eels captured prey by biting them. While a suction feeder can begin physically influencing the prey with the onset of water flow that begins with the onset of buccal expansion, moray eels do not appear to physically interact with the prey until their upper and lower jaws come in contact with the prey during the bite. This difference in prey capture mechanism, biting versus producing suction, appears to be associated with a relaxation in temporal constraints on eel feeding kinematics that are usually present in the kinematics of suction feeders. The loss of suction in morays is associated with greater variation in kinematic movement patterns, which may contribute to the ability of these elongate predatory fish to capture prey exceeding the size of a suction feeder's flow field.
Our prediction that the pattern of moray eel feeding kinematics is less
constrained than that of suction feeders was supported by the finding that
kinematic variance in the morays was significantly higher than
Anguilla, centrarchids and cichlid
(Table 1). In addition to this
difference in overall kinematic variation, morays frequently showed reversals
of head and jaw rotation during the expansive phase of the strike, something
that to our knowledge has never been reported in a suction-feeding fish. The
relative timing and continuous movement of head and jaw excursion creates
unidirectional water flow into the buccal cavity of suction feeders
(Lauder, 1980a;
Lauder and Clark, 1984;
Ferry-Graham and Lauder, 2001;
Ferry-Graham et al., 2003).
Temporary reversals in head and jaw rotation would substantially disrupt the
development of suction-feeding flow patterns because the water flow is so
intimately tied to buccal expansion.
The reduction of the hyoid bar, sternohyoideus muscle and pectoral girdle,
together with the absence of hyoid depression and the absence of suction as a
prey capture strategy, represent a radical departure from the nearly
ubiquitous reliance on hyobranchial depression and suction feeding among
teleost fishes. We speculate that the anatomical modifications seen in the
morays have greatly reduced their suction-feeding ability. In suction-feeding
fish, the cross-sectional area of the hyoid bar must be relatively thick in
order to withstand the forces exerted by a well-developed sternohyoideus
muscle, which delivers an expansive force to the buccal cavity during suction
production (Wainwright et al.,
2006). In morays, it is unlikely that the sternohyoideus muscle
delivers any major expansive forces to the buccal cavity because the muscle is
not only reduced, but the slender hyoid bar does not seem able to withstand
the forces necessary to depress the ventral region of the buccal cavity or
counteract the forces exerted by the epaxialis during dorsal rotation of the
neurocranium (Carroll et al.,
2004). This is further supported by the fact the A.
rostrata, which is more closely related to morays than to the other three
perciform fish used in this study, shares some skull modifications with morays
but has a robust hyoid system and used suction to capture prey. Also, the
tarpon, Megalops atlanticus, an elopomorph member of the sistergroup
to anguilliforms, uses suction to capture prey, has a large hyoid bar, and
reaches peak gape in about 40 ms (Grubich,
2001).
In A. rostrata, the two centrarchids and cichlid included in this
study, and in other suction-feeding teleosts that have been described, the
pectoral girdle forms a robust skeletal foundation for the actions of the
sternohyoideus muscle that originates on the anterior face of the cleithrum
and inserts on the medial region of the hyoid. The sternohyoideus can depress
the hyoid by its contractions, or act as an antagonist to cranial elevation,
also resulting in hyoid depression (Carroll
and Wainwright, 2006). Echidna nebulosa and M.
retifera possess a highly reduced pectoral girdle and while the
sternohyoideus muscle is present, it is small with its primary origin in the
anterior hypaxial muscles. Manual, posteriorly and ventrally directed tension
on the sternohyoideus of fresh specimens of the two moray species revealed
that this action cannot depress the floor of the buccal cavity, as it does in
A. rostrata, centrarchids and cichlids, because the hyoid is held
within the tissues forming the floor of the buccal cavity and is too flexible
to transmit this motion. The rami of the hyoid bar are thin and bent readily
when the floor of the buccal cavity was manually depressed.
Although it was not measured in our lateral-view videos, we did observe
lateral rotation of the suspensoria during moray eel feeding. Suspensorial
abduction is a key component of buccal expansion in most teleosts
(Lauder, 1985) that is
retained in moray eels, along with a well developed levator arcus palantini
muscle that is positioned to abduct the suspensorium. Lateral motion of the
suspensorium was observed in morays during respiration, but in spite of this
ability to expand the buccal cavity somewhat by suspensorium abduction, these
movements appeared to be too slow to result in sufficient suction flow
velocities to move prey items.
Some authors have suggested that the absence of measurable suction distance
may underestimate the role of suction in prey capture, if the predator is
using suction to compensate for forward movement of the body during the strike
(Aerts et al., 2001;
Summers et al., 1998).
However, compensatory suction is unlikely to be a major component of feeding
in morays because of the unusual shape of the moray mouth. Suction-feeding
teleosts are often observed to have a planar, almost circular mouth aperture
(Higham et al., 2006a;
Van Wassenbergh et al., 2006).
The mouth opening of moray eels always reveals a distinctive, deep lateral
notch that exposes most of the mandibular tooth row when seen in lateral view
(Figs 1 and
2). The left and right
mandibles form an anterior apex such that the majority of the mouth aperture
is oriented laterally. We suspect that anterior motion of the moray head with
the jaws abducted results in water spilling out the posterior-lateral part of
the mouth opening. This unusual jaw morphology and mouth shape may result in a
greatly reduced bow wave, possibly eliminating the need for compensatory
suction, and allowing morays to move their jaws into a biting position without
pushing potential prey away from the opened mouth.
Implications for alternative feeding strategies
Moray eels are dominant predators in many coral reef communities
(Carr and Hixon, 1995;
Parrish et al., 1986). The
alternative prey acquisition behavior, biting, has a number of implications
for prey capture kinematics and for feeding biology in this highly successful
lineage. Whether fishes rely on suction or use a ram–suction strategy,
the sequence of cranial events is conserved and the relative timing of
kinematic events appears to be highly constrained to a period of less then 100
ms. In this study, all timing variables and jaw rotation variables loaded
together on the first principal component, clearly separating morays from
A. rostrata. A. rostrata clustered tightly together on both PC1
(magnitude of angular rotation and timing) and PC2 (jaw and head reversals),
indicating that suction production relies on a more restricted range of head
movements (Fig. 5). Studies of
prey capture kinematics in other suction-feeding teleosts have revealed
similar patterns, also suggesting that tight integration of head movements is
a general feature of suction-feeding kinematics (reviewed in
Gibb and Ferry-Graham, 2005).
The present study suggests that biting results in less integrated, and more
temporally variable feeding patterns. Moray eels exhibited longer prey capture
cycles and reversals of jaw and head movements during feeding events. The
frequency of jaw and head reversals during moray feeding sequences was not
correlated with capture times and may be involved in attempts by morays to
track their prey while they position posterior regions of their body for the
strike. Whether jaw and head reversals are associated with prey detection and
tracking necessitates further investigation.
What selection pressures may have shaped the extensive use of biting rather
than suction during prey acquisition in moray eels? In order for suction
feeding to be effective, the predator must place itself directly in front of
the prey item so that the prey is contained within the volume of water that is
captured during the suction-feeding strike
(Higham et al., 2006a). Body
elongation coupled with the active hunting strategies of morays may have
played some role in the loss of suction feeding. Moray eels live within the
deep recesses of rocky and coral reefs where they hunt in confined spaces.
Biting has been suggested as a strategy for overcoming restrictions that
maximum gape size places on diet (Alfaro et
al., 2001). Studies of moray stomach contents indicate that they
prey upon cephalopods, crabs, shrimp and fishes, often consuming relatively
large prey items (Randall,
1967; Randall,
1985; Young and Winn,
2003). Suction feeding may be of limited effectiveness for
capturing particularly large prey that can easily escape the flow field in
front of a moray's mouth. Suction feeding presumably works best when the prey
is small enough to fit within the volume of water contained within one mouth
diameter away from the predator's mouth
(Day et al., 2005;
Higham et al., 2006a;
Van Leeuwen, 1984). Reliance
on directly biting prey rather than capturing prey with suction may represent
an important behavioral adaptation enabling morays to subdue relatively large
prey in confined spaces.
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Aerts, P., van Damme, J. and Herrel, A. (2001). Intrinsic mechanics and control of fast cranio-cervical movements in aquatic feeding turtles. Am. Zool. 41,1299 -1310.[CrossRef]
Alfaro, M. E., Janovetz, J. and Westneat, M. W. (2001). Motor control across trophic strategies: muscle activity of biting and suction feeding fishes. Am. Zool. 41,1266 -1279.[CrossRef]
Anker, G. (1974). Morphology and kinetics of the stickleback, Gastrosteus aculeatus. Trans. Zool. Soc. Lond. 32,311 -416.
Böhlke, E. B., McCosker, J. E. and Böhlke, J. E. (1989). Family Muraenidae. In Fishes of the Western North Atlantic. Pt 9, Vol. 1 (ed. E. B. Böhlke), pp. 104-206. New Haven, CT: Sears Foundation for Marine Research.
Carr, M. H. and Hixon, M. A. (1995). Predation effects on early post-settlement survivorship of coral-reef fishes. Mar. Ecol. Prog. Ser. 124, 31-42.
Carroll, A. M. and Wainwright, P. C. (2006). Muscle function and power output during suction feeding in largemouth bass, Micropterus salmoides. Comp. Biochem. Physiol. 143A,389 -399.[CrossRef]
Carroll, A. M., Wainwright, P. C., Huskey, S. H., Collar, D. C.
and Turingan, R. G. (2004). Morphology predicts suction
feeding performance in centrarchid fishes. J. Exp.
Biol. 207,3873
-3881.
Day, S. W., Higham, T. E., Cheer, A. Y. and Wainwright, P.
C. (2005). Spatial and temporal flow patterns during suction
feeding of bluegill sunfish (Lepomis macrochirus) by Particle Image
Velocimetry. J. Exp. Biol.
208,2661
-2671.
De Visser, J. and Barel, C. D. N. (1998). The expansion apparatus in fish heads, a 3-D kinetic deduction. Neth. J. Zool. 48,361 -395.
Dingerkus, G. and Uhler, L. D. (1977). Enzyme clearing of alcian blue stained whole small vertebrates for demonstration of cartilage. Stain. Technol. 52,229 -232.[Medline]
Ferry-Graham, L. A. and Lauder, G. V. (2001). Aquatic prey capture in ray-finned fishes: a century of progress and new directions. J. Morphol. 248,99 -119.[CrossRef][Medline]
Ferry-Graham, L. A., Wainwright, P. C. and Lauder, G. V. (2003). Quantification of flow during suction feeding in bluegill sunfish. Zool. 106,159 -168.[CrossRef]
Fielitz, C. (2002). Previously unreported pectoral bones in moray eels (Anguilliformes: Muraenidae). Copeia 2002,483 -488.[CrossRef]
Gibb, A. C. and Ferry-Graham, L. A. (2005). Cranial movements during suction feeding in teleost fishes: are they modified to enhance suction production? Zoology Jena 108,141 -153.
Gregory, W. K. (1933). Fish skulls: a study of the evolution of natural mechanisms. Trans. Am. Philos. Soc. 23,75 -481.
Grubich, J. R. (2001). Prey capture in Actinopterygian fishes: a review of suction feeding motor patterns with new evidence from an Elopomorph fish, Megalops atlanticus. Am. Zool. 41,1258 -1261.[CrossRef]
Higham, T. E., Day, S. W. and Wainwright, P. C.
(2005). Sucking while swimming: evaluating the effects of ram
speed on suction generation in bluegill sunfish (Lepomis macrochirus)
using digital particle image velocimetry. J. Exp.
Biol. 208,2653
-2660.
Higham, T. E., Day, S. W. and Wainwright, P. C.
(2006a). Multidimensional analysis of suction feeding performance
in fishes: fluid speed, acceleration, strike accuracy and the ingested volume
of water. J. Exp. Biol.
209,2713
-2725.
Higham, T. E., Hulsey, D. C., 
í
an, O. and
Carroll, A. M. (2006b). Feeding with speed: prey capture
evolution in cichlids. J. Evol. Biol. doi:10.1111/j/1420-9101.2006.01227.x
.
Janovetz, J. (2005). Functional morphology of
feeding in the scale-eating specialist Cataprion mento. J. Exp.
Biol. 208,4757
-4768.
Konow, N. and Bellwood, D. R. (2005).
Prey-capture in Pomacanthus semicirculatus (Teleostei,
Pomacanthidae): functional implications of intramandibular joints in marine
angelfishes. J. Exp. Biol.
208,1421
-1433.
Lauder, G. V. (1980a). The suction feeding
mechanism in sunfishes (Lepomis): an experimental analysis.
J. Exp. Biol. 88,49
-72.
Lauder, G. V. (1980b). Evolution of the feeding mechanism in primitive actinopterygian fishes: a functional anatomical analysis of Polypterus, Lepisosteus, and Amia. J. Morphol. 163,283 -317.[CrossRef]
Lauder, G. V. (1983). Food capture. In Fish Biomechanics (ed. P. W. Webb and D. Weihs), pp.280 -311. New York: Praeger Publishers.
Lauder, G. V. (1985). Aquatic feeding in lower vertebrates. In Functional Vertebrate Morphology (ed. M. Hildebrand, D. M. Bramble, K. F. Liem and D. B. Wake), pp.210 -229. Cambridge, MA: Belknap Press.
Lauder, G. V. and Clark, B. D. (1984). Water
flow patterns during prey capture by teleost fishes. J. Exp.
Biol. 113,143
-150.
Lauder, G. V. and Norton, S. F. (1980).
Asymmetrical muscle activity during feeding in the gar, Lepisosteus
oculeatus. J. Exp. Biol. 84,17
-32.
Liem, K. F. (1980). Acquisition of energy by teleosts: adaptive mechanisms and evolutionary patterns. In Environmental Physiology of Fishes (ed. M. A. Ali), pp. 299-334. New York: Plenum Press.
Muller, M. (1989). A quantitative theory of expected volume change in the mouth during feeding in teleost fishes. J. Zool. Lond. 217,639 -662.
Muller, M., Osse, J. W. M. and Verhagen, J. H. G. (1982). A quantitative hydrodynamical model of suction feeding in fish. J. Theor. Biol. 95, 49-79.[CrossRef]
Nelson, J. S. (2006). Fishes of the World (4th edn). Hoboken, NJ: John-Wiley.
Norton, S. F. and Brainerd, E. L. (1993). Convergence in the feeding mechanics of ecomorphologically similar species in the Centrarchidae and Cichlidae. J. Exp. Biol. 176, 11-29.[Abstract]
Page, L. M. and Burr, B. M. (1991). A Field Guide to Freshwater Fishes of North America north of Mexico. Boston: Houghton Mifflin Company.
Parrish, J. D., Norris, J. E., Callahan, M. W., Callahan, J. K., Magarifuji, E. J. and Schroeder, R. E. (1986). Piscivory in a coral reef fish community. Environ. Biol. Fishes 14,285 -297.
Porter, H. T. and Motta, P. J. (2004). A comparison of strike and prey capture kinematics of three species of piscivorous fishes: Florida gar (Lepisosteus platyrhincus), redfin needlefish (Strongylura notata), and great barracuda (Sphyraena barracuda). Mar. Biol. 145,989 -1000.[CrossRef]
Randall, J. E. (1967). Food habits of reef fishes of the West Indies. Stud. Trop. Oceanogr. 5, 665-847.
Randall, J. E. (1985). Guide to Hawaiian Reef Fishes. Newtown Square, PA: Harrowood Books.
Rice, A. N. and Westneat, M. W. (2005).
Coordination of feeding, locomotor and visual systems in parrottishes
(Teleostei: Labridae). J. Exp. Biol.
208,3503
-3518.
Richard, B. A. and Wainwright, P. C. (1995). Scaling the feeding mechanism of largemouth bass (Micropterus salmoides): kinematics of prey capture. J. Exp. Biol. 198,419 -433.
Sanford, C. P. J. and Wainwright, P. C. (2002). Use of sonomicrometry demonstrates link between prey capture kinematics and suction pressure in largemouth bass. J. Exp. Biol. 205,3445 -3457.
Summers, A. P., Darouian, K. F., Richmond, A. M. and Brainerd, E. L. (1998). Kinematics of aquatic and terrestrial prey capture in Terrapene carolina, with implications for the evolution of feeding in cyptodire turtles. J. Exp. Zool. 281,280 -287.[CrossRef][Medline]
Svanbäck, R., Wainwright, P. C. and Ferry-Graham, L. A. (2002). Linking cranial kinematics, buccal pressure and suction feeding performance in largemouth bass. Physiol. Biochem. Zool. 75,532 -543.[CrossRef][Medline]
Van Leeuwen, J. L. (1984). A quantitative study of flow in prey capture by rainbow trout, with general consideration of the actinopterygian feeding mechanism. Trans. Zool. Soc. Lond. 37,171 -227.
Van Leeuwen, J. L. and Muller, M. (1984). Optimum sucking techniques for predatory fish. Trans. Zool. Soc. Lond. 37,137 -169.
Van Wassenbergh, S., Aerts, P. and Herrel, A.
(2005). Scaling of suction-feeding kinematics and dynamics in the
African catfish, Clarias gariepinus. J. Exp. Biol.
208,2103
-2114.
Van Wassenbergh, S., Aerts, P. and Herrel, A. (2006). Hydrodynamic modeling of aquatic suction performance and intra-oral pressures: limitations for comparative studies. J. R. Soc. Interface 3,507 -514.[CrossRef][Medline]
Wainwright, P. C. and Bellwood, D. R. (2002). Ecomorphology of feeding in coral reef fishes. In Coral Reef Fishes. Dynamics and Diversity in a Complex Ecosystem (ed. P. F. Sale), pp. 33-55. San Diego: Academic Press.
Wainwright, P. C. and Shaw, S. S. (1999). Morphological basis of kinematic diversity in feeding sunfishes. J. Exp. Biol. 202,3101 -3110.[Abstract]
Wainwright, P. C., Ferry-Graham, L. A., Waltzek, T. B., Carroll,
A. M., Hulsey, C. D. and Grubich, J. R. (2001). Evaluating
the use of ram and suction during prey capture by cichlid fishes.
J. Exp. Biol. 204,3039
-3051.
Wainwright, P. C., Huskey, S. H., Turingan, R. G. and Carroll, A. M. (2006). Ontogeny of suction feeding capacity in snook, Centropomus undecimalis. J. Exp. Zool. A 305,246 -252.
Westneat, M. W. (1994). Transmission of force and velocity in the feeding mechanisms of labrid fishes. Zoomorphology 114,103 -118.[CrossRef]
Young, R. F. and Winn, H. E. (2003). Activity patterns, diet, and shelter site use for two species of moray eels, Gymnothorax moringa and Gymnothorax vicinus, in Belize. Copeia 2003,44 -55.[CrossRef]
Yukihira, H., Shibuno, T., Hashimoto, H. and Gushima, K. (1994). Feeding habits of moray eels (Pisces: Muraenidae) at Kuchierabu-jima. Appl. Biol. Sci. 33,159 -166.
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