Coordination of feeding, locomotor and visual systems in parrotfishes (Teleostei: Labridae)
1 Department of Organismal Biology and Anatomy, The University of Chicago,
Chicago, IL 60637, USA
2 Department of Zoology, Field Museum of Natural History, Chicago, IL 60605,
USA
* Author for correspondence (e-mail: arice{at}uchicago.edu)
Accepted 6 July 2005
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Summary |
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Key words: herbivory, kinematics, biomechanics, functional morphology, eye movements, sensorimotor integration, coral reef fish, parrotfish
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Introduction |
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Coordination is the process that integrates the movement of multiple
morphological components of an organism to accomplish a specific task. As each
musculoskeletal system is capable of a nearly infinite range of motions, the
main objective of coordination is to create a functional relationship between
components to reduce the possible range of motion to a narrower range of
motion for the execution of a specific behavior
(Bernstein, 1967;
Turvey, 1990
). In the context
of feeding, coordination involves several functional units, such as locomotor
systems that direct movement and posturing towards the prey item, sensory
systems that detect and guide the animal to the prey, and feeding systems that
capture and process the prey item.
Despite the clear relationship between feeding and swimming, only a few
studies have specifically integrated functional systems in kinematic analyses
in fishes. In the first detailed analysis of locomotor patterns and jaw
movements in fishes, Rand and Lauder
(1981) demonstrated that two
patterns of jaw movement coordinated with two different types of body movement
in pike. Webb (1984a
) found
that during feeding events in several species of freshwater predatory fishes,
approach speed and maneuverability are dependent on morphology of the
locomotor apparatus (paired fins vs body/caudal fin movement), while
body angle of approach is not. Borla et al.
(2002
) demonstrated that
fine-scale maneuverability in larval zebrafish is not dependent upon
appendicular fins alone, but on a combination of body and caudal fin bending
movements, termed fine axial control, to produce a unique swimming style
during prey capture that differs from their normal swimming behavior. Other
studies involving electromyography have looked at motor patterns underlying
movement in combinations of functional systems, such as the firing of jaw and
axial muscles during feeding and escape responses
(Schriefer and Hale, 2004
), or
eye movements during continuous swimming
(Harris, 1965
).
The present study focuses on coordination between feeding systems and the
mechanics of pectoral fin locomotion. Labrid fishes (including wrasses,
parrotfishes and odacids; Westneat and
Alfaro, 2005; Westneat et al.,
2005
) use their pectoral fins as their main propulsors
(Webb, 1984b
;
Westneat, 1996
) to produce a
range of lift- or drag-based propulsion modes
(Westneat, 1996
;
Westneat and Walker, 1997
;
Walker and Westneat, 2000
,
2002b
) that likely play an
important role in feeding behavior. Accompanying the variety in swimming
modes, parrotfishes exhibit browsing, scraping or excavating feeding
strategies to consume algae or detritus
(Ochavillo et al., 1992
;
Bruggemann et al., 1994
;
Streelman et al., 2002
;
Choat et al., 2004
). The
feeding modes of excavating and scraping correspond to specific patterns of
cranial myology (e.g. Board,
1956
; Bellwood and Choat,
1990
; Bullock and Monod,
1997
; Streelman et al.,
2002
) and motor patterns
(Alfaro and Westneat, 1999
).
The diversity of swimming and feeding mechanisms among parrotfishes suggests
that species with different feeding mechanics may employ different
coordination strategies to optimize body movement and positioning for prey
capture.
Sensory systems also play a role in the coordination of feeding. During
feeding, fish eye movements follow predictable patterns, and tracking such
movements can serve as a proxy for visual input during a behavior (Easter and
Nicola, 1996,
1997
;
Rodriguez et al., 2001
). While
swimming, eyes of fishes exhibit compensatory movements to stabilize the
visual field while the body moves
(Trevarthen, 1968
;
Collin and Shand, 2003
), and
there is a close relationship between the periodicity of ocular and locomotor
muscle activity (Harris, 1965
;
Trevarthen, 1968
). In many
fishes, vision serves as the primary source of sensory input used to guide
prey capture and eye movement is quite dramatic before and during the feeding
strike, indicating that visual input is important for prey acquisition
(Pettigrew et al., 2000
;
Anisdon et al., 2001
). Labrid
fishes are assumed to also rely heavily on vision while feeding, though
studies of vision in wrasses have focused primarily on either morphology or
visual pigment sensitivity (Munz,
1958
; Baylor, 1967
;
Barry and Hawryshyn, 1999
;
Siebeck and Marshall, 2000
;
Lara, 2001
), and not on
oculomotor behavior (Tauber and Weitzman,
1969
).
The goal of the present study is to provide a quantitative kinematic analysis of three systems: skull kinesis, locomotion and vision, during feeding behavior in parrotfishes. We ask two primary questions: (1) Are there repeated, stereotypic patterns of coordination between feeding, locomotor and oculomotor systems during a feeding event? Quantitative kinematic data on all three systems allow us to examine levels of variability vs stereotypy in multiple functional systems. (2) How do these coordination patterns differ between species with different feeding ecologies? To address these questions, we present data on feeding coordination in two species of parrotfishes with different scraping and browsing trophic strategies.
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Materials and methods |
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The manner in which prey is presented in analyses of feeding can strongly
influence the behavior and resulting kinematics
(Ferry-Graham et al., 2001).
Scarus were fed commercially prepared frozen algae (Emerald
Entrée, Sally's Bay Brand, Newark, CA, USA) spread on a round piece of
a faviid coral skeleton, and Sparisoma were fed small pieces of
lettuce anchored to the bottom of the tank, extending to the same height as
the coral head treatment. We experimented with standardized prey types, but
neither species would consistently and naturally feed on the preferred food
presentation of the other species. Sparisoma would not eat the algal
smear, and Scarus would only occasionally and passively nip at the
small piece of lettuce. The feeding preference of these species thus required
that we offer them slightly different versions of immobile vegetable matter,
while accounting for as many aspects of the prey presentation as possible,
including height, distance and angle of prey. Trained feeding behaviors of
both species did not seem to differ from natural feeding behaviors observed in
the wild (when observed on SCUBA).
Feeding behaviors were filmed using a digital high-speed video camera
(MotionScope, Redlake Imaging, San Diego, CA, USA) at 250 frames
s-1. Only sequences with a lateral view where the fish could be
clearly seen were analyzed (4 events recorded for each Scarus, 2-3
events for each Sparisoma). A scale-bar was placed over the food item
before the feeding trial to accurately calibrate length in the digitized
footage. Digital video footage was exported as an image sequence (Apple
Quicktime), and imported into TPSdig
(Rohlf, 2003). On each frame
of the video sequence, 19 morphological landmarks were plotted on each image
in order to quantify the movements of the jaws, fins, eyes and body of fishes
during feeding (Fig. 1A).
Landmarks were (1) tip of premaxilla, (2) tip of dentary, (3)
quadrate-articular joint, (4) anterior base of dorsal fin, (5) anterior base
of pelvic fin, (6-9) limits of the orbit, (10-13) limits of the pupil, (14)
leading edge base of pectoral fin, (15) trailing edge base of pectoral fin,
(16) leading edge tip of pectoral fin, (17) trailing edge of median fin ray of
the pectoral fin, (18) trailing tip of pectoral fin, (19) food item (point
closest to the animal).
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Based on the movement of these landmarks, kinematic variables were calculated (Fig. 1B) using a series of algorithms in a custom-written kinematics program (CodeWarrior Pascal, Metrowerks Corporation, Austin, TX, USA) on an Apple Macintosh G5. Variables included distance to prey (linear distance between points 1, 19), body angle of approach (angle created by the line 3, 14, relative to horizontal), gape (distance between points 1 and 2), gape angle (angle 1, 3, 2), jaw protrusion (distance between points 1, 8), cranial elevation (angle 8, 4, 5), pupil distance from the center of the eye (distance between the calculated centers of points 6-9 and 10-13), and pupil angle (angle between the calculated centers of points 6-9 and 10-13, relative to the fish's horizontal axis).
Velocity and acceleration were calculated as first and second derivatives
of time and distance using the QuickSAND program (Walker,
1997,
1998
), and smoothed using the
predicted mean square error quintic spline
(Walker, 1998
). The time that
the fishes first reached the food item was defined as the time of the shortest
distance to the food item, designated as t0 and indicated
as a broken line on kinematic plots. Protraction and abduction of pectoral fin
movement were calculated from the maximum length of the leading edge of the
pectoral fin. Once the maximum length of the fin was determined, we calculated
the projected length (based on the apparent length of the fin ray) into the
z-plane as well as the angle relative to the body using the law of
cosines. Stroke plane angle of the pectoral fins was calculated using the
x,y coordinates of the pectoral fin tip at the beginning and end of a
downstroke. The angle of this line (relative to horizontal) was then
subtracted from the body angle to make the stroke plane angle relative to the
fishes' body position. For comparison, all sequences were aligned based on
t0. Variables are plotted as mean ±
S.E.M.
Coordination of feeding, locomotion and vision was assessed in three ways.
First, we tested for differences between species in single timing variables.
Magnitude, time to maxima, and event duration of the kinematic parameters were
analyzed using a nested ANOVA to test for potential differences between
individuals and species, using the JMP version 5.0.1.2 statistical package
(SAS Institute, Cary, NC, USA). Gape and velocity parameters were scaled by
standard length in statistical analyses to account for the slightly larger
size of the Sparisoma individuals. Second, the overall pattern of
coordination was assessed by comparing the kinematic variables from the three
functional systems relative to the time during the feeding strike. Third, we
examined the stereotypy of kinematic variables to assess the degree to which
feeding coordination was repeated in a similar way from one feeding (or
individual) to the next. Stereotypy of feeding strikes was assessed by
calculating the coefficient of variation (CV) for each individual animal
(Schleidt, 1974;
Barlow, 1977
), and then pooled
for each species to better account for individual variability
(Barlow, 1977
). We predicted
that most cranial kinematics and eye motion would be stereotypic, with CV less
than 1.0, whereas features of fin motion and locomotor and cranial timing
would have higher variability.
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Results |
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Gape distance and gape angle were similar between the two species (Fig. 4A,B). Both magnitude and timing of jaw protrusion were significantly higher in Scarus (Fig. 4C); Scarus also exhibited a second period of jaw protrusion associated with food handling following capture. Strike duration did not differ significantly between the two species (Sparisoma, 0.208±0.012 s; Scarus, 0.204±0.016 s). Sparisoma typically conducted one bite on the food item and then paused for processing, while Scarus exhibited up to five successive bites per feeding bout before pausing for processing. During the strike, cranial elevation was not always present, but when it occurred it was significantly greater in Scarus than Sparisoma (Fig. 4D).
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Both species brake strongly just before biting. A sweeping fin stroke, down and forward, served as a braking maneuver that produced a large decrease in velocity. Braking kinematics of two representative feeding events (Fig. 5A) show that the pectoral braking stroke begins before t0 (prey contact) and extends through the feeding event. Mean braking stroke plots (Fig. 5B) illustrate that Scarus pectoral fins exhibit a significantly larger magnitude of fin protraction during braking (85.1625±8.35°, reaching up to 165°) than Sparisoma (48.287±12.1341°) when the fish bites the food item. The stroke plane angle differed between cruising and braking pectoral fin strokes (Fig. 5C), with Sparisoma sweeping the fins through stroke plane angles for cruising and braking of 70.3±7.7° and 30.7±6.8°, respectively; Scarus cruising was also significantly higher during cruising (67.9±5.5°) than braking (34.4±4.4°).
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Eye movements of the two species followed similar patterns. Upon approach to the prey, the eye was shifted towards the prey item (Sparisoma: 0.0913±0.0101 cm at 173.3±29.1 ms to prey capture; Scarus: 0.1137±0.0147 cm at 178.5±39.4 ms to prey capture), then at approximately 100 ms before food capture the pupil shifted back to a centered position (Fig. 6A). There were no significant differences in either the magnitude or the timing of pupil movement between Sparisoma and Scarus. Pupil movement in both species was forward and slightly downward during the approach in the direction of the prey item. Sparisoma pupils were focused between 0 and -5° (looking slightly downward), while Scarus pupils were focused farther ventrally between -5 and -15° during the approach to the food item (Fig. 6B). At -0.05 s, Scarus pupils returned to a mostly centered position for the bite. When pupil distance is plotted against distance to the food item (Fig. 6C), Sparisoma's eyes shifted to center (2 cm to food contact) before those of Scarus (1 cm to food contact).
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The timing of multiple events was consistently synchronized upon approach to the food item for both species. While there are a large number of possible interactions between kinematic variables, we have chosen examples that illustrate the range of coordination exhibited in parrotfish feeding behavior. Both species used a broadside, braking pectoral fin downstroke just before prey contact that was correlated with a dramatic decrease in velocity (Figs 8A,D, 9A,D). During this deceleration event, the eyes of both species were shifting back to a center-orientation (Figs 8A,C and 9A,C). In Sparisoma, maximum attained velocity is synchronized with maximum gape (Fig. 8A,B), whereas Scarus does not exhibit the same degree of synchrony between these two parameters (Fig. 9A,B). For both Scarus and Sparisoma the maximum distance of the pupil from the center of the eye is synchronized with the onset of mouth opening, but the eyes are shifting to center when the mouth fully opens (Figs 8B,C and 9B,C). In both species, maximum gape coincides with a large fin upstroke, and mouth closing is correlated with a fin downstroke (Figs 8 and 9).
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Discussion |
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Coordination of skull, fins and eyes during fish feeding
Feeding in parrotfishes involves rapid biting of the substrate or algal
prey with coordinated movement of the body, skull, jaws and pectoral fins,
mediated primarily by the use of vision. The common features of feeding
coordination in parrotfishes are evident in the timing patterns of kinematic
parameters (Fig. 10), which
can be divided into three primary phases. First, during the approach phase,
when the fish is still greater than 300 ms from prey contact, both parrotfish
species began to adjust cranial and locomotor features. Approach angle and
pectoral fin motion were modulated to some degree but showed repeated
patterns, with low CV (Fig. 7).
The eyes of both species were maximally shifted forward at approximately 175
ms before prey contact, coinciding with a slight decrease in body angle.
During the strike phase, from about 300 ms pre-contact until the bite,
Scarus began to increase cranial elevation (peaking at 175±32
ms), and at approximately 100 ms to prey contact, jaw protrusion increased
(peaking at 37.3±3.9 ms). Scarus onset of jaw opening occurred
after the onset of jaw protrusion (though maximum gape occurred before maximum
jaw protrusion at 42±0.01 ms before prey contact). In contrast,
Sparisoma delays cranial elevation until much later in the feeding
cycle but initiates jaw opening earlier
(Fig. 10). Most notable is the
difference in the timing between the onset of jaw opening and the achievement
of maximum gape between the two species. Jaw opening initiates the
Sparisoma feeding sequence, followed by cranial elevation, and lastly
jaw protrusion, whereas the Scarus sequence begins with cranial
elevation, followed by jaw protrusion and lastly maximal jaw opening
(Fig. 10). Cranial kinematics
were significantly different between species for the strike phase, with gape
timing, magnitude of jaw protrusion, time to maximum jaw protrusion, cranial
elevation and order of events in the feeding sequence showing interspecific
differences.
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These differences in coordination of the herbivorous bite may be due to
differences in food type. Sparisoma radians eats mainly seagrass
blades and epiphytes (Lobel and Ogden,
1981), while Scarus quoyi consumes mainly benthic turf
algae and associated detritus and bacterial mat
(Ochavillo et al., 1992
). Due
to the physical differences in the morphology of these food items, the
associated functional demands of prey capture (browsing vs scraping)
are consequently different for these two species and are reflected in their
feeding behaviors. The blades of seagrass may be somewhat motile in areas with
current, and by initiating mouth opening first, Sparisoma has
attained maximum gape with the mouth having created a larger area for grabbing
the seagrass blade to compensate for potential minor movements of the grass.
Scarus does not have this need as the benthic turf algae remains at a
fixed point, and instead needs to exert more force during its bite to
successfully scrape algae off of the coral head
(Fig. 9D). Variability in
cranial elevation in parrotfishes studied here was also noted in the EMG study
of Alfaro and Westneat (1999
)
in which variable presence/absence of epaxial muscle activity was shown to be
associated with variable cranial elevation in parrotfishes.
The two species also exhibited different patterns of pectoral fin movement
during the feeding strike. During braking, Scarus quoyi pectoral fins
primarily moved forward during braking (in protraction), whereas Sparisoma
radians pectoral fins primarily moved downward (in abduction) for braking
(Fig. 5,
Table 1). The stroke plane
angle in labriform swimmers may range from almost vertical to nearly
horizontal, and this variable is a primary determinant of the mode of thrust
production by the pectoral fin stroke (Walker and Westneat,
2000,
2002a
). Though the data on
stroke plane angle did not appear to differ between species, further analyses
of steady and unsteady state swimming of these species is needed to confirm
differences in locomotor mechanics. Scarus has a significantly higher
pectoral fin aspect ratio than Sparisoma (data from
Wainwright et al., 2002
;
one-way ANOVA: d.f.=1, F=14.8056, P=0.0009). Fin morphology
is a correlate of the type of labriform locomotion (drag or lift-based;
Westneat, 1996
;
Westneat and Walker, 1997
;
Walker and Westneat, 2000
,
2002a
;
Wainwright et al., 2002
).
These underlying differences in fin morphology and additional possible
differences in musculature may contribute to differences in thrust
production.
The pectoral fins provide thrust for two alternative goals of locomotion
during feeding: maneuvering during feeding bouts and locomotion during
foraging. The pectoral fin protraction of Scarus quoyi during its
bite has longer duration and greater magnitude than that of Sparisoma
(Fig. 5B,C). The extended
downstroke of Scarus may contribute a reactive force that helps move
the jaws across the coral head during the scraping bite, increasing the
efficiency of the scrape, as well as regulating the force of the collision
between the jaws and the substrate. During many Scarus bites, it
appears as though the fish is slamming its head into the rock, and force-plate
technology would be an interesting tool to test this idea. For
Sparisoma feeding on seagrass blades, the large braking maneuver is
not as critical, as these plants do not present a hazard of collision, and
Sparisoma will often swim into and through the sea grass blade as it
bites (as seen in both field and laboratory feeding events). Additionally,
Sparisoma may combine the motions of pectoral fin downstroke and head
movement to help tear pieces from the blades of food. More broadly, the
locomotor strategies may reflect the energetics required for foraging
distances (Wainwright et al.,
2002). The turf algae fed upon by Scarus quoyi is
distributed irregularly across the reef flat and reef slope (e.g.
Ochavillo et al., 1992
), and
consequently, the species would have to spend more time and cover more
distance swimming while foraging. Sparisoma foraging in high density
and broadly distributed beds of seagrass blades
(Lobel and Ogden, 1981
) may
not need increased locomotor efficiency to cover large distances while
feeding.
Although any musculoskeletal system of the body may be involved in
coordinated behavior, such behaviors in vertebrates typically include the
appendages, vertebrae and axial musculature, cranial morphology, and sensory
organs involved in parallel control of movement and posture
(Massion and Dufossé,
1988; Massion,
1992
; Massion et al.,
2003
). Control of movements in any organism can either be
microscopic or macroscopic in scale (muscle cells contracting vs
appendicular or axial movements); simple or complex in scope (such as action
within a single appendage to actions comprised of multiple appendages or body
parts; Bernstein, 1967
;
Clarac, 1984
;
Turvey, 1990
;
Weiss and Jeannerod, 1998
).
Movements are guided by exteroceptive and/or proprioceptive sensory feedback
and must be appropriately synchronized in both temporal and spatial domains
for the task to succeed (Weiss and
Jeannerod, 1998
; Cordo and
Gurfinkel, 2003
). For behaviors involving complex coordination,
voluntary movements are often supported by involuntary (`associated')
movements (Cordo and Gurfinkel,
2003
); for example, movements that serve to adjust the center of
gravity of the organism to compensate for changes in posture
(Massion et al., 2003
). The
coordination of motor systems itself is not the end goal, but a means of
successfully executing a behavior (Weiss
and Jeannerod, 1998
).
These principles of coordinated behavior can be used by the biomechanics
community to collect data on multiple systems in important behaviors such as
feeding and locomotion. For the herbivores studied here, coordinated execution
of fin movement, body posture and jaw movement may be necessary for bouts of
continuous feeding along the floor of the coral reef or sea-grass beds.
Herbivorous reef fishes are suggested to have well-developed pectoral
musculature to precisely move and orient the body during feeding events
(Choat, 1991). Fishes in other
trophic groups (i.e. piscivores and planktivores) also need to integrate these
functional systems during feeding. However, we predict that the coordination
of pectoral fins and their role in maneuverability are less important during
the actual strike of a piscivore, but are prominent during stalking and again
during braking after the strike. The combination of ram and suction feeding
might be sufficient for successful prey capture and decrease the needed
precision of body orientation, as prey items will be swept into the mouth by
the accelerating flow field (Wainwright et
al., 2001
). Herbivores may require a finer level of precision in
coordination in order to graze effectively along substrata with varying
topographies and at varying angles (Webb,
1984b
). Bellwood
(2003
) suggested that the
process of successful food procurement is the main constraint in the evolution
of marine herbivores. Timing the braking maneuver of pectoral fin downstroke
to coordinate with jaw closing will prevent fishes from colliding with their
prey item, and the braking motion would also serve to lift the fish up and
away from the food, allowing the fish to begin food processing, establishing a
posture that promotes predator observation, and reorient to the next location
for biting.
Coordination variability: is the herbivore's bite stereotypic?
Because food type was not altered during these experiments, no dramatic
variations in feeding behaviors were observed
(Fig. 7), but the subtle
differences in feeding mechanics again demonstrate that herbivores have a
range of biting styles (Bellwood and
Choat, 1990; Alfaro and
Westneat, 1999
; Alfaro et al.,
2001
). The kinematic parameters of velocity (Figs
3A,
7A), body angle (Figs
3D,
7A), gape distance (Figs
4A,
7B), gape angle (Figs
4B,
7B) and jaw protrusion (Figs
4C,
7B), fin downstroke (Figs
5B,
7C) and eye movement (Figs
6,
7D) show a relatively low
amount of variability, and thus a high degree of stereotypy, while
acceleration (Figs 3C,
7A), cranial elevation (Figs
4D,
7B), and the fin beat cycle
(Figs 5,
7C) reveal high degrees of
variability. Jaw and eye movements appear to be stereotypic during the feeding
sequence for each species, along with certain features of fin movements (i.e.
braking downstroke), as evidenced by the low variance at individual time
points. Alfaro and Westneat
(1999
) demonstrated variation
in the motor pattern of jaw muscles during feeding between Scarus
iseri and Cetoscarus bicolor, particularly during the multiple
bite bouts of S. iseri. In the present study we found low variability
in the feeding movements in Scarus quoyi and Sparisoma
radians; electromyography data are now being sought to further test the
stereotypy of the motor pattern.
The variability of fin movements might serve as a part of feedback
modulation (sensu Deban et al.,
2001): final adjustments to ensure proper body position and speed
at the point of contact, before a feed-forward motor program is triggered for
the biting behavior. Such modifications of movement would explain the lack of
stereotypic patterns of fin beat patterns during the approach to the prey
item. Only the approach and initial bite were examined for the two species;
the bites for each species appeared to be stereotypic, as opposed to the two
different bites utilized by Scarus iseri
(Alfaro and Westneat, 1999
).
Future studies will analyze the kinematics and coordination of multiple bites
in Scarus quoyi to test for stereotypy or functional versatility in
the repeating bite mode. Exploring the effect of differences in food type
(Sanderson, 1991
) or
ontogenetic stage (Reilly,
1995
; Cook, 1996
;
Deban and Dicke, 1999
) will
further reveal the degree of relative stereotypy of the feeding behavior of
these species.
Intergeneric differences between the feeding behaviors of these
parrotfishes further demonstrates the evolutionary plasticity in the labrid
feeding mechanism (Alfaro and Westneat,
1999; Alfaro et al.,
2001
), and provides supporting evidence for the hypothesis that
differences in feeding ecology are responsible for early diversification among
the parrotfishes (Streelman et al.,
2002
). This difference is probably amplified by specialization on
different food types (Liem,
1978
,
1979
). Such modulation of
feeding behaviors may have allowed for the expansion into and specializations
for different trophic niches (Streelman et
al., 2002
), and observed differences in feeding behaviors, such as
differences in bite rate between Scarus and Sparisoma
(Lobel and Ogden, 1981
;
Bellwood and Choat, 1990
;
Ochavillo et al., 1992
), may
reflect behavioral or physiological adaptations to nutritional differences in
food quality (e.g. Choat,
1991
; Choat and Clements,
1998
; Choat et al.,
2002
).
The role of vision in parrotfish feeding
For both species of parrotfishes, a shift in pupil position from
forward-looking (at the prey) to centered (viewing the environment) occurred
well before actual contact with the food item: approximately 100 ms and 1.75
cm for Sparisoma, and 100 ms and 1 cm from the food item for
Scarus (Fig. 6). The
parrotfish Cryptomus roseus has a temporal foveal depression
(Ali and Anctil, 1976),
suggesting that the near field of vision in parrotfishes is in increased focus
during the approach to the food item
(Fernald and Wright, 1985
;
Fernald, 1990
). In fishes with
specialized areas of the retina, eye movements indicate the visual field of
the fish and where the fish is looking
(Collin and Shand, 2003
). This
analysis of eye movement suggests that although vision is used for guidance to
the prey item, it is not involved in the final execution of the bite. As the
parrotfish gets close to the food item, the jaws or snout of the fish may
block the visual field of the laterally positioned eyes (e.g.
Tamura, 1957
), necessitating
the use of other senses for final prey capture. Sensory input in this close
range may be primarily mediated by the lateral line
(Liem, 1978
;
Janssen and Corcoran, 1993
;
New et al., 2001
;
Montgomery et al., 2002
).
Future work exploring the details of the structure and function of the
parrotfish eye will elaborate the role of the visual system in the coordinated
behavior of these fishes.
The observed lateral eye movement back to a centered position
(Fig. 6) may additionally serve
as a mechanism for predator detection. Parrotfish are vulnerable to predation
(e.g. Randall, 1967;
Overholtzer and Motta, 2000
),
and their head-down foraging position further increases this vulnerability
(Krause and Godin, 1996
;
Overholtzer and Motta, 2000
).
Scarids may also have to avoid attacks from territorial damselfishes when they
feed on algae within their territories
(Ogden and Buckman, 1973
).
Thus, when vision is no longer needed for guidance to a prey item, rapid eye
movements may serve as the first line of defence against predators or
attackers (Endler, 1986
).
Ecomorphology and evolution of multiple functional systems
As the goal of ecomorphology is to link morphology to ecology through
organismal performance (e.g. Wainwright,
1994,
1996
), combined analysis of
the behavior of multiple functional morphological systems may provide a more
accurate estimation of the animal's abilities. Many previous studies of
ecomorphology have focused on a single functional system such as the jaws or
fins (e.g. Liem, 1978
;
Westneat, 1995
;
Wainwright, 1996
;
Wainwright and Bellwood, 2002
;
Wainwright et al., 2002
),
though it is becoming increasingly clear from this study and others that it is
the combination and interaction of these functional systems that truly
determines an animal's ecology
(Ferry-Graham et al., 2002a
;
Wainwright et al., 2002
).
Ferry-Graham et al. (2002a
)
stated that when foraging, an organism has to deal with a series of ecological
`filters', which ultimately determine if and how the organism forages. The
animal has to detect a potential food item (sensory systems), it has to be
able to arrive at the food item (locomotion), and then consume the item
(feeding). In the context of coordination, we suggest that as the organism
feeds, these filters continually place constraints on behavior, and the
interaction of these filters results in coordination. Simultaneous analysis
and quantification of multiple components of coordinated behavior may
elucidate the interface between functional morphology, biomechanics and
feeding ecology.
Despite the once-perceived functional homogeneity of herbivorous fishes
(see Choat, 1991), comparative
studies are demonstrating diversity and specializations for niche partitioning
in these fish groups (Bruggemann et al.,
1994
). Coordination analysis may provide a complementary and
integrative approach to previous studies of parrotfish feeding morphology
(Board, 1956
; Tedman,
1980a
,b
;
Clements and Bellwood, 1988
;
Bellwood and Choat, 1990
;
Monod et al., 1994
;
Bullock and Monod, 1997
),
locomotor morphology (e.g. Westneat,
1996
; Bellwood and Wainwright,
2001
; Wainwright et al.,
2002
), ecology (Ogden and
Buckman, 1973
; Lobel and
Ogden, 1981
; Ochavillo et al.,
1992
; Bruggemann et al.,
1994
) and evolution (Bellwood,
1994
; Bernardi et al.,
2000
; Streelman et al.,
2002
). By placing swimming, feeding and sensory function in the
same context of feeding behavior, it is possible to document alternative
combinations of functional parameters that might provide further axes of
diversification between organisms that share a similar food source.
Similarly, coordination analysis holds promise for exploring the feeding
strategy of closely related species in different trophic guilds. Within the
Labridae, the parrotfishes represent one end of the trophic ecology continuum
(Westneat, 1995;
Wainwright and Bellwood, 2002
;
Wainwright et al., 2004
).
Thus, a comparison of how these functional systems interact in species of this
family that consume different prey types may elucidate coordination
differences necessary for different trophic niches. Additionally, further
comparisons of sensory system function between fishes of different trophic
types may reveal the functional constraints of particular feeding strategies,
such as prey detection vs predator detection. Analyses of multiple
functional systems within the context of coordination during feeding behaviors
will further reveal axes of differentiation for feeding ecology in sympatric
species to partition trophic resources within a community.
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