|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online February 15, 2008
Journal of Experimental Biology 211, 699-708 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.009852
Feeding kinematics, suction and hydraulic jetting capabilities in bearded seals (Erignathus barbatus)
1 Texas A&M University at Galveston, Department of Marine Biology, 5007
Avenue U, Galveston, TX 77551, USA
2 Norwegian Polar Institute, N-9296 Tromsø, Norway
* Author for correspondence (e-mail: marshalc{at}tamug.edu)
Accepted 6 December 2007
 |
Summary |
|---|
 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Key words: pinnipeds, feeding kinematics, suction feeding
|
INTRODUCTION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
; Muller et al.,
1982; Lauder,
1985; Deban and Wake,
2000; Wainwright et al.,
2007; Wilga et al.,
2007). Prey is ingested from a distance by inducing water flow
into the oral cavity through rapid jaw opening and buccal cavity expansion.
Our knowledge of the detailed hydrodynamics of suction feeding has recently
been advanced greatly for ray-finned fishes (e.g.
Sanford and Wainwright, 2002;
Svanback et al., 2002;
Ferry-Graham et al., 2003;
Carroll, 2004;
Carroll et al., 2004;
Day et al., 2005;
Higham et al., 2005;
Van Wassenbergh et al., 2005;
Van Wassenbergh et al., 2006;
Higham et al., 2006a;
Higham et al., 2006b;
Holzman et al., 2007;
Wainwright and Day, 2007;
Wainwright et al., 2007) and
for chondrichthyans (e.g. Motta et al.,
2002; Matott et al.,
2005; Sasko et al.,
2006; Dean et al.,
2007; Nauwelaerts et al.,
2007; Wilga et al.,
2007). Significant work has been conducted for salamanders, which
exhibit a diversity of intermediate stages between unidirectional and
bidirectional suction feeding (Lauder and
Shaffer, 1986; Shaffer and
Lauder, 1985; Lauder and
Reilly, 1988; Reilly and
Lauder, 1988; Shaffer and
Lauder, 1988; Miller and
Larsen, 1989; Reilly and
Lauder, 1990; Reilly and
Lauder, 1992; Lauder and
Shaffer, 1993; Deban and Wake,
2000), and for turtles and anurans
(Lauder and Prendergast, 1992;
Bels et al., 1997;
Summers et al., 1997;
Van Damme and Aerts, 1997;
Deban and Olsen, 2002;
Mason, 2003). This body of
work has demonstrated that aquatic prey capture using inertial suction is
conserved in the sequence and timing of events over a wide range of taxa.
These similarities in kinematic patterns are thought to be a result of life in
an aquatic medium; the density and viscosity of water imparts strong selection
pressures for inertial suction feeding
(Lauder, 1985). However, among
secondarily derived tetrapods, particularly aquatic mammals, few
investigations of suction feeding have been conducted. Although anatomical
data for the feeding apparatus among aquatic mammals are numerous, only a few
experimental investigations of feeding behavior have been conducted
(Kastelein and Mosterd, 1989;
Kastelein et al., 1994;
Kastelein et al., 1997;
Marshall et al., 1998;
Werth, 2000a;
Marshall et al., 2003;
Bloodworth and Marshall; 2005;
Werth 2006a). Among pinnipeds,
experimental feeding data are available only for walruses (Odobenus
rosmarus), which are known to excel at suction feeding and demonstrate an
effective excavation technique involving the alternation of suction and
hydraulic jetting (forceful ejection of water out of the mouth; the opposite
behavior to suction) to consume bivalves
(Fay, 1982;
Kastelein and Mosterd, 1989;
Kastelein et al., 1994).
The feeding behavior and trophic ecology of bearded seals (Erignathus
barbatus Erxleben 1777) are thought to be similar to walruses, and
suction is presumed to be the primary feeding mode in this species
(King, 1983), although there
are no data to support or refute this statement. Bearded seals are the largest
of the arctic phocids, and their biology was poorly known until recently
because they are pagophilic, inhabit remote regions where the ice is in
constant motion, and they occur at low densities
(Burns, 1981). However, during
the past decade concerted efforts have greatly increased our knowledge of
bearded seal natural history, and their importance to arctic ecosystems (e.g.
Hammill et al., 1994;
Lydersen et al., 1994;
Kovacs et al., 1996;
Lydersen et al., 1996;
Andersen et al., 1999;
Lydersen and Kovacs, 1999;
Gjertz et al., 2000;
Krafft et al., 2000;
Lydersen et al., 2001;
Marshall et al., 2001;
Van Parijs et al., 2001;
Lydersen et al., 2002;
Van Parijs et al., 2003;
Van Parijs et al., 2004;
Davies et al., 2006;
Marshall et al., 2006;
Van Parijs and Clark, 2006;
Dehn et al., 2007;
Risch et al., 2007). Analyses
of stomach contents and recent stable isotope analyses demonstrate that
bearded seals are generalist foragers (e.g.
Hjelset et al., 1999;
Dehn, 2007), and are the only
northern phocid that feeds predominantly on benthic prey, including
crustaceans, mollusks, infaunal worms and benthic fish; the importance of each
group varies regionally (Chapskii,
1938; Pikharev,
1940; Vibe, 1950;
Kenyon, 1962;
Johnson et al., 1966;
Kosygin, 1966;
Burns, 1967;
Kosygin, 1971;
Lowry et al., 1980;
Burns, 1981;
Finley and Evans, 1983;
Hjelset et al., 1999).
Owing to their size and suction feeding capability, bearded seals are excellent subjects to investigate suction performance in phocids. However, to date, suction feeding in this species has not been studied. Additionally, pinniped suction feeding has not been characterized within the context of vertebrate evolution. Bearded seals are probably important ecological components of arctic benthic ecosystems because of their potential for causing substantial bioturbation during foraging, similar to walruses, and hence this feeding modality warrants investigation in a broad ecological context. Therefore, the objectives of this study were to (1) investigate feeding behavior in bearded seals to determine the range of their behavioral repertoire for capturing prey and to determine if suction feeding is the primary feeding mode in this species, as opposed to biting, (2) determine if bearded seal suction performance is similar to values reported for walruses, and (3) compare suction feeding in bearded seals with other vertebrates.
|
MATERIALS AND METHODS |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
4 cm long and 2 cm wide) of herring were used in the study because this
was the food that the subjects consume on a daily basis. Prior to the study
all subjects were individually fed a ration of cut herring by hand. All work
was conducted under Texas A&M University's Institute of Animal Care and
Use Committee Animal Use Protocol #2003-89 and in accordance with animal care
guidelines within Norway.
Feeding platforms
Three feeding apparatuses were constructed to present food items to
subjects in a controlled manner. The primary feeding apparatus was constructed
from wood and PlexiglasTM. A mirror, sandwiched between PlexiglasTM
and plywood, was placed behind the feeding surface at a 45° angle to
provide simultaneous frontal and lateral views of the muzzle, jaw, and
vibrissae during feeding events. The subjects were presented with food items
using a sheet of PlexiglasTM that was inserted vertically into the
feeding platform with the face parallel to the camera's perspective
(Fig. 1). Cut fish pieces were
presented to the subjects in two ways, simultaneously. Thirty holes, 2.5 cm in
diameter, were drilled through the PlexiglasTM in six rows and five
columns, approximately 2 cm apart. Cut fish pieces were pushed through the
holes such that portions of the fish projected 3 cm from the feeding
surface, and were accessible to the subjects. In addition, cut fish pieces
were placed within eight recessed PlexiglasTM wells (cylinders) that were
positioned behind several of the holes through the PlexiglasTM. Holes of
1 cm diameter were drilled through the back of the PlexiglasTM wells to
allow water to flow through. The feeding apparatus was suspended in the pool
approximately 1 m below the surface of the water, with the PlexiglasTM in
the vertical plane. A halogen light (500 W) was suspended over the feeding
apparatus to illuminate the feeding surface and the subject's face. Feeding
trials were also conducted with the feeding platform on land. Subjects hauled
out pool-side to feed from the apparatus in the same manner as during the
in-water trials.
|
|
By presenting food items projecting from holes in the feeding surface and within the recessed wells during feeding trials using the primary feeding apparatus, subjects were forced to make several choices when presented with food. Upon encountering food items, their first choice was whether to consume fish projecting from the holes or fish residing within the recessed wells. If seals chose to consume fish projecting from holes in the PlexiglasTM feeding surface, then they had to choose whether to consume the piece of fish by biting and removing the fish with their teeth, or to use suction. If a subject chose to consume a piece of fish in the recessed well, then its only option was to use suction to obtain the food item. In this way it was possible to determine whether subjects used biting or suction as their primary feeding mode. In addition, food was presented to the subjects in the feeding apparatus such that the feeding surface was vertical, or horizontal; the latter most closely mimicked benthic foraging. Plastic tubing was attached to the back of one of the recessed wells so that dark green food coloring could be injected into the cylinder to visualize water flow generated by the subjects.
Feeding trials, kinematic variables and analyses
A feeding trial was defined as a single presentation to a subject of food
items inserted into the PlexiglasTM feeding surface. Several trials were
conducted each day, and feeding trials spanned a 2 week period, in each of the
2 years; pressure measurements were made only in year 2 of the experiment. A
feeding event was defined as a single measurable ingestion of a food item.
Therefore, a single feeding trial could produce numerous feeding events. A
total of 133 feeding trials were analyzed to assess preferred feeding mode.
Among these trials, 42 feeding events (14 lateral on-land trials, N=7
per subject; 14 lateral in-water trials, N=7 per subject, and 14
frontal in-water trials, N=7 per subject) were chosen for kinematic
analyses based on the criteria that both subject and prey were visible in the
video frame, all landmarks were visible during the trial, and rotation of the
body was minimal (less than 15°). Subjects were videotaped (30 frames per
second) using a Sony TRV 900 or 950 camcorder. Prior to feeding trials, zinc
oxide was placed on the subject's lips, jaws and head to provide high contrast
landmarks for digitizing. Landmarks were digitized frame-by-frame for motion
analysis using Vicon Motus 9.0 motion analysis software system (Denver, CO,
USA), which separates frames into individual fields to provide a 60 Hz record.
Kinematic variables measured were: (1) maximum gape, the maximum distance from
upper jaw tip to lower jaw tip; (2) time to maximum gape, the time from when
the lower jaw began to open until maximum gape; (3) maximum gape angle, the
maximum angle from the maxillary tip to corner of the mouth to mandibular tip;
(4) time to maximum gape angle; the time from when the lower jaw began to open
until maximum gape angle; (5) maximum opening gape angle velocity, the
greatest angular rate of lower jaw opening; (6) time to opening gape angle
velocity, the time from when the lower jaw began to open until maximum gape
angle velocity was achieved; (7) maximum closing gape angle velocity, the
greatest angular velocity during lower jaw closure; (8) time to maximum
closing gape angle velocity, the time from when the lower jaw began to close
until maximum gape angle velocity was achieved; (9) maximum hyoid depression,
the greatest increase in distance from the eye to external rostral border of
the hyoid apparatus visible externally; (10) time to maximum hyoid depression,
the time from the start of hyoid depression to maximum hyoid depression
relative to the eye; (11) velocity of food transport, and (12) gape cycle
duration.
Pressure measurements
A total of 363 suction and 42 hydraulic jetting events generated by
subjects were characterized using a Millar MPC-500 catheter pressure
transducer connected to a transducer control box (TCB-600; Houston, TX, USA)
and a Biopac MP150 portable electrophysiological recording system (Oleta, CA,
USA). Electrophysiological data were saved to a MacIntosh iBook hard-drive.
The pressure transducer was calibrated by inserting the distal end into a
sealed flask and varying the pressure from –80 kPa to 0 kPa using a
certified vacuum hand pump. Voltage output of the pressure transducer was
linear across the entire pressure range (r2=0.99).
Differential values of pressure traces from feeding trials were inspected
through time, and analyzed using Acknowledge software (Oleta, CA, USA).
Inspection of pressure traces prior to analysis ensured that noise artifacts
were avoided. Furthermore, only pressure measurements that exceeded 0.1 V in
magnitude were included in the data analysis.
Pressure measurements were collected using the smallest feeding apparatus;
pressure was measured only underwater. A pressure transducer was placed
through the back of a recessed well (that contained the food) so that the tip
of the transducer, where the recording element was located, projected
approximately 2 cm beyond the PlexiglasTM feeding surface. This allowed
the pressure sensor to be just at the seal's lips, or slightly within the oral
cavity, during feeding. Control over the distance between the pressure
transducer element and the lips of the subject was important since suction
forces are inversely proportional to distance
(Svanback et al., 2002;
Ferry-Graham et al., 2003).
This distance was verified visually during all feeding trials, and verified on
the video footage. Only suction data from feeding trials in which the tip of
the transducer was in contact with the lips of the subject, or within the oral
cavity, were used in this study. Suction measurements collected in these
feeding trials were: (1) the duration of the preparatory phase, a short
suprambient pressure trace prior to a suction event verified by video (2) the
maximum suprambient pressure during the preparatory phase, (3) duration of the
subambient pressure drop, (4) the maximum subambient pressure, (5) duration of
the change from maximum subambient pressure to ambient pressure, and (6)
entire duration of the suction profile. Hydraulic jetting measurements
collected were: (1) duration of the superambient pressure increase, (2) the
maximum suprambient pressure, (3) duration of the change from maximum
suprambient pressure to ambient pressure, (4) entire duration of the hydraulic
jetting pressure profile.
Statistics
Normality of data was tested using a Kolmogorov–Smirnov test.
Levene's test was used to test the assumption of homogeneity of variances. All
kinematic and pressure data were log10 transformed to normalize
variances. Log10-transformed kinematic variables were used in a
one-way analysis of variance (ANOVA), with the kinematic variables as the
dependent factors and location (on land vs in water) as the
independent factor, to determine the differences between kinematic profiles of
suction vs biting. Pearson's `r' correlation analyses
assessed the positive or negative relatedness of the timing and displacement
variables of feeding events. All statistical tests were conducted using SPSS
14.0 for the PC.
|
RESULTS |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
In-water feeding trials yielded markedly different results from on-land
feeding trials. Underwater, the subjects used suction exclusively whether or
not food was projecting from a hole, or located within a recessed well. When
food items within recessed wells were difficult to extract, subjects would
employ suction, and alternate this behavior with hydraulic jetting. This
behavior was evident when pieces of fish would oscillate back-and-forth within
the recessed well until enough force was employed to remove it. The fact that
suction, and not biting, was being used, even when feeding from the recessed
wells, was clearly evident from the reduced gape (confirmed by kinematics, see
below), pursing of the lips to form a circular aperture, sealing of the lips
to occlude lateral gape, and the lack of lip curling and observation of teeth.
Alternating suction with hydraulic jetting was successful for extracting
difficult-to-get food because holes in the PlexiglasTM were slightly
narrower than the diameter of the PlexiglasTM cylinder, which created a
small bottleneck (2 mm). The alternation of suction with hydraulic
jetting resulted in small changes in the position of fish pieces within the
cylinder that allowed food to be extracted through this small bottleneck.
Further evidence that suction and hydraulic jetting were being used
alternately was the appearance of air bubbles from turbulence flowing from the
back of the recessed wells toward the subject's lips during suction events,
alternating with cloudy plumes of minute fish particles and scales exiting the
back of the recessed wells during hydraulic jetting events. Also, during
experiments in which food color was injected into a recessed well to visualize
water, water flow clearly alternated in direction, depending upon whether
suction or hydraulic jetting was being employed. Lastly, these suction and
hydraulic jetting behaviors were confirmed during the pressure transducer
experiments (see below).
During in-water feeding trials, suction behavior dominated, constituting 96.3% of feeding behaviors; no biting behavior was observed underwater (N=17 trials). The remaining 3.7% of behaviors were hydraulic jetting events. During analyses of the first year's data, it became evident that the frequency of hydraulic jetting behaviors depended on the number of fish pieces inserted per recessed well. Therefore, during the second year, a series of feeding trials (N=30) in which only recessed wells were used was conducted. Each recessed well was filled with a minimum of two pieces of fish, with the intent of making the extraction of fish as difficult as possible. Placing fish in the recessed wells in this manner increased the frequency of hydraulic jetting behaviors. Since all fish items were placed within the recessed wells, biting was not an option for subjects to obtain food items during these trials. These feeding trials resulted in suction and hydraulic behavior frequencies of 86% and 14%, respectively.
Use of vibrissae
Mystacial vibrissae were used during both on-land and underwater feeding
trials. On land, subjects appeared to use vision to search and find food
items, but always resorted to using vibrissae to center the mouth over the
food. Subjects closed their eyes during this last centering step. Underwater,
vision appeared to be used little if at all at close range; the vibrissae were
used to search for food and center the mouth over the food item. Once the
seals were searching for food on the feeding apparatuses, their eyes were
always closed and their vibrissae were everted. The vibrissae were brought
from a state of relaxation to an active state in which they were spread apart,
directed forward of the rostrum, and used to scan the PlexiglasTM feeding
surface. Although it is difficult to ascertain conclusively, it appeared the
seals were able to use vibrissae to detect either the opening of a recessed
well or a small piece of fish protruding from the well. Individual and
multiple vibrissal deflections were often observed as the whiskers moved over,
or into, a recessed opening. Subjects usually moved immediately in the
direction of these vibrissal deflections.
Feeding kinematics
Four feeding phases: (I) preparatory, (II) jaw opening, (III) hyoid
depression and (IV) jaw closing were observed regardless of the feeding mode.
During suction feeding (in-water trials) the mean durations for phase
I–IV were, 0.06 s (s.d. ±0.06), 0.21±0.09 s,
0.16±0.05 s and 0.11±0.05 s, respectively. During biting
(on-land trials), the mean duration for phases I–IV were
0.06±0.03 s, 0.13±0.06 s, 0.18±0.08 s and
0.15±0.05 s, respectively. The preparatory phase involved closing of
the mouth prior to jaw opening, and adduction of the hyoid. The duration of
hyoid depression overlapped with phases II and IV. The mean feeding cycle
duration was 0.53±0.21 s, and was not significantly different between
suction and biting feeding modes (P>0.05, ANOVA). However, motion
analysis data strongly supported differences in the kinematics of suction
versus biting feeding (Table
1, Fig. 3), and
supported the behavioral data on suction and biting feeding behavior. In
general, suction was characterized by a small gape (2.7±0.85 cm) and
gape angle (24.4±8.13°), whereas biting was characterized by a
large gape (7.3±2.2 cm) and gape angle (41.7±15.2°). Both
gape and gape angle were significantly different between suction and biting
(P<0.01 and 0.01, respectively, ANOVA). Time to maximum gape and
time to maximum gape angle were not significantly different between suction
and biting (P>0.05; t-test). Displacement and temporal
measures of maximum gape and maximum gape angle during in-water feeding trials
were not significantly different between frontal and lateral feeding trials
(P>0.05; t-test), and these data were pooled with similar
measurements from the lateral perspective (N=28). During all feeding
trials, maximum hyoid depression always occurred after maximum gape; maximum
hyoid depression was significantly greater during suction than biting
(P<0.01, ANOVA). Not surprisingly, maximum opening gape angle
velocity was significantly different between suction and biting
(204.76±92.4 deg. s–1 and 328±176 deg.
s–1, respectively; P<0.05, ANOVA), as were time
to maximum opening gape angle velocity (0.10±0.04 s and
0.17±0.07 s; P<0.01, ANOVA) and time to closing gape angle
velocity (0.08±0.03 s and 0.16±0.10 s; P<0.01,
ANOVA). Kinematic variables of biting and suction feeding are summarized in
Table 1.
|
|
A Pearson's correlation analysis further supported these differences between suction and biting feeding kinematics (Table 2). Feeding site (feeding mode) was significantly correlated with maximum hyoid depression (negatively), maximum gape, maximum gape angle, maximum opening gape angle velocity, time to opening gape angle velocity, and time to closing gape angle velocity. Maximum hyoid depression was negatively correlated with maximum gape. Smaller hyoid depression and greater gape resulted in biting, whereas greater hyoid depression and small gape resulted in suction feeding. Time to maximum hyoid depression was correlated with time to maximum gape, and time to maximum gape angle highlighting the synchronization of these movements. Time to maximum hyoid depression was also negatively correlated with maximum closing gape angle velocity. Food velocity was significantly correlated to time to maximum opening gape angle velocity.
|
Suction and hydraulic jetting pressures
Bearded seals used both suction and hydraulic jetting when feeding from any
of the feeding platforms during in-water trials. The electrophysiological data
(Fig. 4A) demonstrated that
suction events comprised three phases: a preparatory phase, a expansive phase
(during which maximum subambient pressure occurred) and a compressive phase.
The preparatory phase was always characterized by a small suprambient pulse in
pressure. The mean magnitude and duration of preparatory phases were
3.78±2.58 kPa and 0.10±0.04 s, respectively. The expansive phase
was characterized by a rapid (0.15±0.085 s) subambient drop in
pressure. The maximum subambient measurement recorded was 91.2 kPa. The
compressive phase was characterized by a rapid (0.12±0.096 s) return of
pressure to the baseline values. The duration of the expansion phase was
significantly longer than the duration of the compression phase
(P<0.01, t-test). Pressure traces of hydraulic jetting
(Fig. 4B) demonstrated only a
rapid compressive phase (0.055±0.034 s) and expansive phase
(0.051±0.028 s); a preparatory phase was never observed. The mean
durations of the compressive and expansive phases during hydraulic jetting
were not significantly different (P>0.05, t-test); the
maximum suprambient measurement recorded during hydraulic jetting was 54 kPa.
Mean hydraulic jetting duration (0.11±0.055 s) was significantly
shorter than the mean suction duration (0.26±0.11 s;
P<0.01, t-test).
|
|
DISCUSSION |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
;
Marshall et al., 2003;
Bloodworth and Marshall, 2005).
Eye closure may serve to increase the tactile sensory modality, by closing
down their visual sense. Psychophysical data suggests that increased direction
of attention within a particular sensory modality enhances that sense, but can
result in a decrease in stimulus processing of other modalities
(Kawashima et al., 1995;
Spence, 2002;
Marx et al., 2003).
Alternatively, eye closure may be a protective function for bearded seals
feeding in the wild in substrates that are potentially abrasive to the
eye.
The suction generation mechanism in bearded seals, and probably all aquatic
mammals, is limited to rapid jaw opening and depression of the hyolingual
complex (Werth, 2000a;
Werth, 2000b;
Bloodworth and Marshall, 2005;
Bloodworth and Marshall, 2007;
Werth, 2007). This mechanism
differs considerably from cranial elevation observed in ray-finned fishes in
which the amount of force from the epaxial musculature is correlated with the
magnitude of the pressure produced [as well as other parameters
(Carroll, 2004;
Wainwright et al., 2007)].
Rapid jaw opening, and hyolingual depression, is probably widespread among
suction feeding aquatic mammals, but few comparative data are available. The
maximum opening gape angle velocity for bearded seals (204 deg.
s–1) is similar to values reported for pygmy and dwarf sperm
whales (Kogia spp.; 293 deg. s–1), the latter a
known suction feeder (Bloodworth and
Marshall, 2005). By contrast, the maximum opening gape angle
velocity in bottlenose dolphins (Tursiops truncatus), a known ram
feeder, was reported to be 84 deg. s–1
(Bloodworth and Marshall,
2005). In aquatic mammals that presumably use suction extensively,
the tongue functions as a cylindrical piston that is rapidly depressed and
retracted to produce subambient pressures
(Werth, 2000b;
Werth, 2006a;
Werth, 2007). Interestingly,
the use of the tongue in hyolingual depression in aquatic mammals is a
departure from the presence of tongues in adult postmetamorphic salamanders,
which usually signifies a terrestrial feeding mode
(Lauder and Shaffer, 1993;
Deban and Wake, 2000). Time to
maximum hyoid depression for bearded seals (0.3 s) is similar to values
reported for pygmy and dwarf sperm whales [0.28 s
(Bloodworth and Marshall,
2005)], and pilot whales [Globicephala melas; 0.45 s
(Werth, 2000a)]. Conversely,
time to maximum hyoid (gular) depression for bottlenose dolphins was reported
to be 0.62 s [pooled data (Bloodworth and
Marshall, 2005)]. Although the function of the hyolingual complex
in pinnipeds has not received much attention, the hyolingual apparatuses of
presumed suction feeding odontocetes (toothed whales) are robust, and
hyolingual muscles have relatively large cross-sectional areas
(Reidenberg and Laitman, 1994;
Werth, 2007). However, among
marine mammals the orofacial morphology, tongue morphology, and the rapidity
of hyolingual depression may be more important in generating suction than the
force produced by hyolingual muscles
(Bloodworth and Marshall, 2005;
Bloodworth and Marshall, 2007).
Several modifications of the orofacial morphology (e.g. short blunt rostra and
mandible, reduced dentition) and hyolingual complex (short, broad tongues) are
hypothesized to enhance suction performance in odontocetes
(Reidenberg and Laitman, 1994;
Marshall et al., 2001;
Werth, 2000a;
Werth, 2000b;
Bloodworth and Marshall, 2005;
Werth, 2006b;
Bloodworth and Marshall, 2007;
Werth, 2007). Bearded seals,
and possibly all pinnipeds that use suction to feed, also have short, broad
snouts and jaws that presumably increase suction performance. The mobile and
muscular muzzle and lips of bearded seals occlude the sides of the mouth,
blocking lateral gape, and direct water flow toward the rostral lips. The
rostral lips simultaneously purse to form a circular aperture through which
water flows. The function of the lateral lips is analogous to the membranous
labial lips that span the jaws in suction feeding ray-finned fishes
(Lauder, 1979), the labial
lobes of suction feeding salamanders
(Lauder and Shaffer, 1986;
Lauder and Reilly, 1988;
Miller and Larsen, 1989;
Deban and Wake, 2000), and the
labial cartilages of suction feeding elasmobranchs
(Motta et al., 2002;
Matott et al., 2005;
Wilga et al., 2007). The
pursing of the rostral lips is convergent with the shape of the mouths of
suction feeding fishes, and salamanders
(Deban and Wake, 2000;
Wainwright et al., 2007).
Modifications of the orofacial morphology in bearded seals (and odontocetes)
supports the general premise that differences in peripheral morphology are
correlated with increased suction performance among aquatic vertebrates
(Lauder and Shaffer, 1986;
Lauder and Shaffer, 1993).
Bearded seals modulated their feeding kinematics between aquatic and
terrestrial environments, mainly through differences in gape, gape angle,
hyoid depression, and maximum opening gape angle velocity. Cryptodire turtles
(Summers et al., 1997) and
adult tiger salamanders [Ambystoma tigrinum
(Lauder and Shaffer, 1986;
Shaffer and Lauder, 1988)]
also exhibit a reduction in hyoid depression when feeding in a terrestrial
environment. Although, bearded seal gape cycle and time to maximum gape did
not differ significantly between aquatic and terrestrial environments, gape
during biting was greater than during suction, which explains the increased
opening gape angle velocity on land vs in water. The differing
density and viscosity of the two environments also probably influences this
variable.
Pressure traces of the preparatory phase were usually characterized by a
small suprambient pulse in pressure, which suggests that subjects were pushing
their tongues up to the hard palate to expel any intraoral water. The
adduction of the hyolingual complex would increase intraoral volume
displacement during hyoid depression, thus increasing suction capability.
Ray-finned fishes are also known to exhibit hyoid adduction, and a
super-ambient pulse in pressure, during a preparatory phase
(Lauder, 1980;
Lauder, 1985;
Nemeth, 1997). As in other
suction feeding vertebrates, depression of the hyoid apparatus in bearded
seals is important in generating subambient pressures. The maximum subambient
pressure measured in bearded seals (91.9 kPa) is comparable to data collected
from walruses by Fay [91.2 kPa (Fay,
1982)] and Kastelein et al. [51–118 kPa
(Kastelein et al., 1994)], and
higher than odontocetes (Kastelein et al.,
1997; Werth,
2006a), all of which are more massive than bearded seals.
A significant finding of this study was that bearded seals exhibited an
excavation behavior (alternation of suction and hydraulic jetting) similar to
walruses (Fay, 1982;
Kastelein and Mosterd, 1989;
Born et al., 2003;
Levermann et al., 2003). On
average, the duration of bearded seal suction events was rapid relative to
walruses (0.27 s vs 0.77–1.06 s, respectively), which probably
reflect differences in maximum subambient pressures between the two pinnipeds.
Longer durations of suction and hydraulic jetting events in bearded seals
resulted in greater sub- or suprambient pressures recorded. A similar
relationship between duration and maximum sub- and suprambient pressures was
also reported in tiger salamanders (Lauder
and Shaffer, 1986). Different durations of suction events in
bearded seals and walruses probably reflect real differences in foraging
ecology. Most bearded seal prey are epibenthic, or shallow infaunal species,
whereas walruses are specialized infaunal molluscivores that target mature,
large, deeply burrowing bivalves [e.g. Mya spp.
(Fay, 1982)]. It is probable
that large bivalves resist being preyed upon by walruses, and require a longer
handling (suction duration) time. However, generally speaking, feeding data
presented in this study support the claim that bearded seal feeding and
foraging is similar to that of walruses
(King, 1983).
Investigations of suction feeding in bearded seals provide new data for a
previously undocumented vertebrate group, the Phocidae, regarding the
convergence evolution of suction feeding behavior by vertebrates. In general,
the kinematics of suction feeding in bearded seals is similar to other suction
feeders across a diverse array of lineages. The bidirectional flow of water
during suction feeding in bearded seals (and probably all aquatic mammals), is
most similar to postmetamorphic salamanders that have lost their gills, and
gill slits (Lauder and Shaffer,
1986; Shaffer and Lauder,
1988; Deban and Wake,
2000). Unlike fish, the volume of the buccal cavity in bearded
seals is limited, and the ingested volume of water should equal the ejected
volume of water. Seals differ from other bidirectional suction feeders
(inertial or compensatory) in that they are not known to exhibit behaviors
that are analogous to buccopharyngeal expansion as observed in turtles
(Van Damme and Aerts, 1997;
Lemell et al., 2002), nor are
they known to posses structures similar to a postglottal pharynx in pipid
frogs (Mason, 2003). Although,
it is generally thought that suction feeding in bidirectional systems is less
efficient than unidirectional systems
(Lauder and Shaffer, 1986;
Shaffer and Lauder, 1988;
Reilly and Lauder, 1988) (but
see Miller and Larsen, 1989),
inertial suction feeding by bearded seals demonstrates that mammalian
bidirectional suction feeders can generate substantial subambient pressures.
However, this may be simply due to relative species size, and a
correspondingly large, buccal volume.
Despite differences in the mechanisms of suction generation among aquatic
animals, the hydrodynamics of suction should be similar across all
vertebrates, including seals. Suction hydrodynamics are best known among
ray-finned fishes (e.g. Sanford and
Wainwright, 2002; Ferry-Graham
et al., 2003; Carroll et al.,
2004; Day et al.,
2005; Higham et al.,
2005; Van Wassenbergh et al.,
2005; Van Wassenbergh et al.,
2006; Higham et al.,
2006a; Higham et al.,
2006b; Holzman et al.,
2007; Wainwright and Day,
2007; Wainwright et al.,
2007). In ray-finned fishes, the size and shape of the buccal
cavity influence the relationship between peak pressure and fluid velocity
(Van Wassenbergh et al.,
2006), but peak pressure drop is usually in close agreement with
peak fluid velocity (Higham et al.,
2006b). The velocity, acceleration of fluid flow, pressure
gradient and effective distance of fluid flow are related to the size of the
mouth aperture (Ferry-Graham et al.,
2003; Higham et al.,
2006a; Higham et al.,
2006b; Wainwright and Day,
2007; Wainwright et al.,
2007). Suction feeding imparts three forces on the prey: drag,
pressure gradient and acceleration reaction. Pressure gradient is the largest
of these forces (Wainwright and Day,
2007), and prey capture is more successful when the pressure
gradient is steeper. Steep pressure gradients can be accomplished by either
increasing the rate of fluid velocity, or by restricting the size of the mouth
aperture (Wainwright and Day,
2007). The large and rapid maximum subambient pressures, and the
relatively small aperture of bearded seals, should result in a steep gradient
in pressure that imparts sizeable forces on their prey items. Suction feeding
performance of bearded seals is analagous to that of bluegill sunfish
(Lepomis macrochirus). Bluegill sunfishes generate a higher fluid
speed and higher fluid acceleration than largemouth bass (Micropterus
salmoides), in the earthbound reference, whereas largemouth bass generate
a higher volume flow and higher volume flow rate
(Higham et al., 2006b). The
higher fluid speed and acceleration in bluegill sunfishes is related to their
narrow mouth aperture, and their ability to focus their suction generation
more in front of the mouth, resulting in greater accuracy. Bearded seals
probably share these characteristics. A trade-off probably exists between the
ability to generate higher fluid speeds and higher volumetric flow rate
[without taking ram feeding into account
(Higham et al., 2006b)].
Vertebrates that generate high fluid speed should also possess small mouths,
with an ability to deliver high force to buccal expansion
(Higham et al., 2006b).
Suction performance data of bearded seals presented here supports this
prediction. Their mouth aperture is relatively small and directed forward, the
rapid depression of the hyolingual apparatus delivers force for buccal
expansion, and the intraoral pressures measured were high relatively to other
aquatic mammals. Furthermore, bearded seals target relatively non-elusive
prey, most of which are benthic and epibenthic. Bearded seals probably exhibit
high fluid flow and a steep pressure gradient, which are advantageous for
feeding upon benthic prey.
Bearded seals feeding on marine worms within infaunal tubes could use the
substrate and the cylindrical geometry of the worm tubes to passively increase
suction distance. The positive effect of the substrate passively increasing
the suction distance of benthic foragers has been documented in both
ray-finned and chondrichthyan fishes
(Carroll et al., 2004;
Nauwelaerts et al., 2007).
Although significant fluid velocities during suction events in ray-finned
fishes are usually confined to a region within one mouth width from the mouth
(Ferry-Graham et al., 2003;
Day et al., 2005),
visualization of water flow around the mouth of benthic foraging bamboo sharks
(Chiloscyllium plagiosum) demonstrated that the boundary of the flow
field can be passively increased up to 2.5 times the mouth width distance,
because of the effect of the substrate
(Nauwelaerts et al., 2007).
Bearded seals feeding on marine tube worms may benefit not only from the
effect of the substrate on fluid flow into the mouth during suction, but may
be able to further extend the boundary of the flow field beyond the effect of
the substrate due to the cylindrical geometry of infaunal tubes.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Andersen, M., Hjelset, A. M., Gjertz, I., Lydersen, C. and Gulliksen, B. (1999). Growth, age at sexual maturity and condition in bearded seals (Erignathus barbatus) from Svalbard, Norway. Polar Biol. 21,179 -185.[CrossRef]
Bels, V. L., Davenport, J. and Delheusy, V. (1997). Kinematic analysis of the feeding behavior in the box turtle Terrapene carolina (L.) (Reptilia:Emydidae). J. Exp. Zool. 277,198 -212.[CrossRef]
Bloodworth, B. and Marshall, C. D. (2005).
Feeding kinematics of Kogia and Tursiops (Odonticeti:
Cetacea): characterization of suction and ram feeding. J. Exp.
Biol. 208,3721
-3730.
Bloodworth, B. and Marshall, C. D. (2007). A functional comparison of the hyolingual complex in pygmy and dwarf sperm whales (Kogia breviceps and K. sima), and bottlenose dolphins (Tursiops truncatus). J. Anat. 211, 78-91.[CrossRef][Medline]
Born, E. W., Rysgaard, S., Ehlme, G., Sejr, M., Acquarone, M. and Levermann, N. (2003). Underwater observations of foraging free-living Atlantic walruses (Odobenus rosmarus rosmarus) and estimates of their food consumption. Polar Biol. 26,348 -357.
Burns, J. J. (1967). The Pacific Bearded Seal. Juneau: Alaska Department of Fish and Game.
Burns, J. J. (1981). Bearded Seal Erignathus barbatus, Erxleben, 1777. In Handbook of Marine Mammals, Vol. 2, Seals (ed. S. H. Ridgway and R. J. Harrison), pp. 145-170. London: Academic Press.
Carroll, A. M. (2004). Muscle activation and
strain during suction feeding in the largemouth bass, Micropterus
salmoides. J. Exp. Biol.
207,983
-991.
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.
Chapskii, K. K. (1938). The bearded seal (Erignathus barbatus, Fabr.) of the Kara and Barents Seas. Trans. Arctic Inst. Leningrad 123, 7-70.
Davies, C., Kovacs, K. M., Lydersen, C. and VanParijs, S. M. (2006). Ontogeny of display behaviour in captive male bearded seals (Erignathus barbatus). Mar. Mamm. Sci. 22,952 -965.[CrossRef]
Day, S. W., Higham, T. E., Cheer, A. Y. and Wainwright, P.
C. (2005). Spatial and temporal patterns of water flow
generated by suction-feeding bluegill sunfish Lepomis macrochirus
resolved by particle image velocimetry. J. Exp. Biol.
208,2661
-2671.
Dean, M. N., Bizzarro, J. J. and Summers, A. P.
(2007). The evolution of cranial design, diet, and feeding
mechanisms in batoid fishes. Integr. Comp. Biol.
47, 70-79.
Deban, S. M. and Olsen, W. M. (2002). Suction feeding by a tiny predatory tadpole. Nature 420, 41-42.[CrossRef][Medline]
Deban, S. M. and Wake, D. B. (2000). Aquatic feeding in salamanders. In Feeding (ed. K. Schwenk), pp. 65-94. San Diego: Academic Press.
Dehn, L. A., Sheffield, G. G., Follmann, E. H., Duffy, L. K., Thomas, D. L. and O'Hara, T. M. (2007). Feeding ecology of phocid seals and some walrus in the Alaskan and Canadian Arctic as determined by stomach contents and stable isotope analysis. Polar Biol. 30,167 -181.[CrossRef]
Fay, F. H. (1982). Ecology and Biology of the Pacific Walrus, Odobenus rosmarus divergens Illiger (North American Fauna, No. 74). Washington DC: US Department of the Interior, Fish and Wildlife Service.
Ferry-Graham, L., Wainwright, P. C. and Lauder, G. V. (2003). Quantification of flow during suction feeding in bluegill sunfish. Zoology 106,159 -168.[CrossRef][Medline]
Finley, K. J. and Evans, C. R. (1983). Summer diet of the bearded seal (Erignathus barbatus) in the Canadian High Arctic. Arctic 36,82 -89.
Gjertz, I., Kovacs, K. M., Lydersen, C. and Wiig, Ø. (2000). Movements and diving of bearded seal (Erignathus barbatus) mother and pups during lactation and post-weaning. Polar Biol. 23,559 -566.[CrossRef]
Hammill, M. O., Kovacs, K. M. and Lydersen, C. (1994). Local movements by nursing bearded seal (Erignathus barbatus) pups in Kongsfjorden, Svalbard. Polar Biol. 14,569 -570.
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., Day, S. W. and Wainwright, P. C.
(2006b). The pressures of suction feeding: the relation between
buccal pressure and induced fluid speed in centrarchid fishes. J.
Exp. Biol. 209,3281
-3287.
Hjelset, A. M., Andersen, M., Gjertz. I., Lydersen, C. and Gulliksen, G. (1999). Feeding habits of bearded seals (Erignathus barbatus) from the Svalbard area, Norway. Polar Biol. 21,186 -193.[CrossRef]
Holzman, R., Day, S. W. and Wainwright, P. C.
(2007). Timing is everything: coordination of strike kinematics
affects the force exerted by suction feeding fish on attached prey.
J. Exp. Biol. 210,3328
-2226.
Johnson, M. L., Fiscus, C. H., Ostenson, B. T. and Barbour, M. L. (1966). Marine mammals. In Environment of the Cape Thompson Region, Alaska (ed. N. J. Wilimovsky and J. N. Wolfe), pp. 897-924. Oak Ridge, TN: US Atomic Energy Commission.
Kastelein, R. A. and Mosterd, P. (1989). The excavation technique for molluscs of Pacific Walrusses (Odobenus rosmarus divergens) under controlled conditions. Aquat. Mamm. 15,3 -5.
Kastelein, R. A., Muller, M. and Terlouw, A. (1994). Oral suction of a Pacific walrus (Odobenus rosmarus divergens) in air and under water. Z. Säugetierk. 59,105 -115.
Kastelein, R. A., Staal, C., Terlouw, A. and Muller, M. (1997). Pressure change in the mouth of a feeding harbor porpoise Phocoena phocoena). In The Biology of the Harbor Porpoise (ed. A. J. Read, P. R. Wiepkema and P. E. Nachtigall), pp. 279-291. Woerden: DeSpil Publishers.
Kawashima, R., O'Sullivan, B. T. and Roland, P. E.
(1995). Positron-emission tomography studies of cross-modality
inhibition in selective attentional tasks: Closing the mind's eye.
Proc. Natl. Acad. Sci. USA
92,5969
-5972.
Kenyon, K. W. (1962). Notes on the phocid seals at Little Diomede Island, Alaska. J. Wildl. Manage. 26,380 -387.[CrossRef]
King, J. E. (1983). Seals of the World (3rd edn). Ithaca: Cornell University Press.
Kosygin, G. M. (1966). Some data on the feeding of the bearded seals in Bering Sea during the spring-summer months. Izv. TINRO 58,153 -157.
Kosygin, G. M. (1971). Feeding of the bearded seal Erignathus barbatus nauticus (Pallas) in the Bering Sea during the spring-summer period. Izv. TINRO 75,144 -151.
Kovacs, K. M., Lydersen, C. and Gjertz, I. (1996). Birth site characteristics and prenatal molting in bearded seals (Erignathus barbatus). J. Mamm. 77,1085 -1091.[CrossRef]
Krafft, B. A., Lydersen, C., Kovacs, K. M., Gjertz, I. and Haug, T. (2000). Diving behaviour of lactating bearded seals (Erignathus barbatus) in the Svalbard area. Can. J. Zool. 78,1408 -1418.[CrossRef]
Lauder, G. V. (1979). Feeding mechanisms in primitive teleosts and in the halecomorph fish Amia calva. J. Zool. Lond. 187,543 -578.
Lauder, G. V. (1980). The suction feeding
mechanism in sunfishes (Lepomis): an experimental analysis.
J. Exp. Biol. 88,49
-72.
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: Harvard University Press.
Lauder, G. V. and Prendergast, T. (1992).
Kinematics of aquatic prey capture in the snapping turtle Chelydra
serpentina. J. Exp. Biol.
164, 55-78.
Lauder, G. V. and Reilly, S. M. (1988).
Functional design of the feeding mechanism in salamander: causal bases of
ontogenetic changes in function. J. Exp. Biol.
134,219
-233.
Lauder, G. V. and Shaffer, H. B. (1986). Functional design of the feeding mechanism in lower vertebrates: unidirection and bidirectional flow systems in the tiger salamander. Zool. J. Linn. Soc. 88,277 -290.[CrossRef]
Lauder, G. V. and Shaffer, H. B. (1993). Design of feeding system in aquatic vertebrates: major patterns and their evolutionary interpretations. In The Skull: Functional and Evolutionary Patterns. Vol. 3 (ed. J. Hanken and B. K. Hall), pp. 113-149. Chicago: University of Chicago Press.
Lemell, P., Lemell, C., Snelderwaard, P., Gumpenberger, M.,
Wocheslander, R. and Weisgram, J. (2002). Feeding patterns of
Chelus fimbriatus (Pleurodira:Chelidae) J. Exp.
Biol. 205,1495
-1506.
Levermann, N., Galatius, A., Ehlme, G., Rysgaard, S. and Born, E. W. (2003). Feeding behaviour of free-living walruses with notes on apparent dextrality of flipper use. BMC Ecol. 3, 1-13.[Medline]
Lowry, L. F., Frost, K. J. and Burns, J. J. (1980). Feeding of bearded seals in the Bering and Chukchi seas and trophic interaction with Pacific walruses. Arctic 33,330 -342.
Lydersen, C. and Kovacs, K. M. (1999). Behaviour and energetics of ice-breeding, North Atlantic phocid seals during the lactation period. Mar. Ecol. Prog. Ser. 187,265 -281.[CrossRef]
Lydersen, C., Hammill, M. O. and Kovacs, K. M. (1994). Diving activity in nursing bearded seal (Erignathus barbatus) pups. Can. J. Zool. 72, 96-103.[CrossRef]
Lydersen, C., Kovacs, K. M., Hammill, M. O. and Gjertz, I. (1996). Energy intake and utilization by nursing bearded seal (Erignathus barbatus) pups from Svalbard, Norway. J. Comp. Physiol. B 166,405 -411.[CrossRef][Medline]
Lydersen, C., Kovacs, K. M. and Lydersen, E. (2001). Rust-colored bearded (Erignathus barbatus) and ringed (Phoca hispida) seals from Svalbard, Norway. J. Mamm. 82,225 -230.[CrossRef]
Lydersen, C., Kovacs, K. M., Ries, S. and Knauth, M. (2002). Precocial diving and patent foramen ovale in bearded seal (Erignathus barbatus) pups. J. Comp. Physiol. B 172,713 -717.[CrossRef][Medline]
Marshall, C. D., Huth, G. D., Edmonds, V. M., Halin, D. L. and Reep, R. L. (1998). Prehensile use of perioral bristles during feeding and associated behaviors of the Florida manatee (Trichechus manatus latirostris). Mar. Mamm. Sci. 14,274 -289.[CrossRef]
Marshall, C. D., Kovacs, K. M. and Lydersen, C. (2001). Morphology of the Bearded Seal (Erignathus barbatus) Muscular-Vibrissal Complex. 14th Biennial Conference on the Biology of Marine Mammals, Vancouver, British Columbia.
Marshall, C. D., Maeda, H., Iwata, M., Furuta, M., Asano, A., Rosas, F. and Reep, R. L. (2003). Orofacial morphology and feeding behaviour of the dugong, Amazonian, West African and Antillean manatees (Mammalia: Sirenia): functional morphology of the muscular-vibrissal complex. J. Zool. Lond. 259, 1-16.[CrossRef]
Marshall, C. D., Amin, H., Kovacs, K. M. and Lydersen, C. (2006). Microstructure and innervation of the vibrissal follicle-sinus complex in the bearded seal, Erignathus barbatus (Pinnipedia: Phocidae). Anat. Rec. A 288, 13-25.[Medline]
Marx, E., Stephan, T., Note, A., Deutschländer, A., Seelos, K. C., Dieterich, M. and Brandt, T. (2003). Eye closure in darkness animates sensory systems. NeuroImage 19,924 -934.[CrossRef][Medline]
Mason, D. (2003). Suction feeding in the pipid frog, Hymenochrus boettgeri: kinematic and behavioral considerations. Copeia 2003,879 -886.[CrossRef]
Matott, M. P., Motta, P. J. and Hueter, R. E. (2005). Modulation in feeding kinematics and motor pattern of the nurse shark Ginglymostoma cirratum. Environ. Biol. Fishes 74,163 -174.[CrossRef]
Miller, B. T. and Larsen, J. H. (1989). Feeding performance in aquatic postmetamorphic newts (Urodela:Salamandridae): are bidirectional flow systems necessarily inefficient? Can. J. Zool. 67,2414 -2421.
Motta, P. J., Hueter, R. E., Tricas, T. C. and Summers, A. P. (2002). Kinematic analysis of suction feeding in the nurse shark, Ginglymostoma cirratum (Orectolobiformes, Ginglymostomatidae). Copeia 2002,24 -38.[CrossRef]
Muller, M., Osse, J. W. M. and Verhage, J. H. G. (1982). A quantitative hydrodynamical model of suction feeding in fish. J. Theor. Biol. 95, 49-79.[CrossRef]
Nauwelaerts, S., Wilga, C. D., Sanford, C. P. and Lauder, G. V. (2007). Substrate passively improves suction feeding in benthic sharks. J. R. Soc. Interface 2, 341-345.[CrossRef]
Nemeth, D. H. (1997). Modulation of buccal pressure during prey capture in Hexagrammos decagrammus (Teleostei: Hexagrammidae). J. Exp. Biol. 200,2145 -2154.[Abstract]
Pikharev, G. A. (1940). Some data on the feeding of the Pacific bearded seal. Izv. TINRO 20,101 -120.
Reidenberg, J. and Laitman, T. L. (1994). Anatomy of the hyoid apparatus in odontoceti (toothed whales): specializations of their skeleton and musculature compared with those of terrestrial mammals. Anat. Rec. 240,598 -624.[CrossRef][Medline]
Reilly, S. M. and Lauder, G. V. (1988). Ontogeny of aquatic feeding performance in the eastern newt, Notophthalmus viridescens (Salamandridae). Copeia 1988,97 -91.
Reilly, S. M. and Lauder, G. V. (1990). The evolution of tetrapod feeding behavior: kinematic homologies in prey transport. Evolution 44,1542 -1557.[CrossRef]
Reilly, S. M. and Lauder, G. V. (1992). Morphology, behavior, and evolution: comparative kinematics of aquatic feeding in salamanders. Brain Behav. Evol. 40,182 -196.[Medline]
Risch, D., Clark, C. W., Corkeron, P. J., Elepfandt, A., Kovacs, K. M., Lydersen, C., Stirling, I. and Van Parijs, S. M. (2007). Call classification and geographical variation in the vocalisations of bearded seals (Erignathus barbatus). Anim. Behav. 73,747 -762.[CrossRef]
Sanford, C. P. J. and Wainwright, P. C. (2002).
Use of sonomicrometry demonstrates the link between prey capture kinematics
and suction pressure in largemouth bass. J. Exp. Biol.
205,3445
-3457.
Sasko, D. E., Dean, M. N., Motta, P. J. and Hueter, R. E. (2006). Prey capture behavior and kinematics of the Atlantic cownose ray, Rhinoptera bonasus. Zoology 109,171 -181.[CrossRef][Medline]
Shaffer, H. B. and Lauder, G. V. (1985). Patterns of variation in aquatic ambystomatid salamander: kinematics of the feeding mechanism. Evolution 39, 83-92.[CrossRef]
Shaffer, H. B. and Lauder, G. V. (1988). The ontogeny of functional design: metamorphosis of feeding behaviours of tiger salamanders (Ambystoma tigrinum). J. Zool. Lond. 216,437 -454.
Spence, C. (2002). Multisensory attention and tactile information-processing. Behav. Brain Res. 135, 57-64.[CrossRef][Medline]
Summers, A. P., Darouian, K. F., Richmond, A. M. and Brainerd, E. L. (1997). Kinematics of aquatic and terrestrial prey capture in Terrapene carolina, with implications for the evolution of feeding in cryptodire turtles. J. Exp. Zool. 281,280 -287.[CrossRef]
Svanback, 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 Damme, J. and Aerts, P. (1997). Kinematics and functional morphology of aquatic feeding in Australian snake-necked turtles (Pleurodira; Chelodina). J. Morphol. 233,113 -125.[CrossRef][Medline]
Van Parijs, S. M. and Clark, C. W. (2006). Long-term mating tactics in an aquatic-mating pinniped, the bearded seal, Erignathus barbatus. Anim. Behav. 72,1269 -1277.[CrossRef]
Van Parijs, S. M., Kovacs, K. M. and Lydersen, C. (2001). Spatial and temporal distribution of vocalizing male bearded seals: implications for male mating strategies. Behaviour 138,905 -922.[CrossRef]
Van Parijs, S. M., Lydersen, C. and Kovacs, K. M. (2003). Vocalizations and movements suggest alternative mating tactics in male bearded seals. Anim. Behav. 65,272 -283.
Van Parijs, S. M., Lydersen, C. and Kovacs, K. M. (2004). The effects of ice cover on the behavioural patterns of aquatic mating male bearded seals. Anim. Behav. 68, 89-96.[CrossRef]
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 modelling of aquatic suction performance and
intra-oral pressures: limitations for comparative studies. J. R.
Soc. Interface 3,507
-514.
Vibe, C. (1950). The marine mammals and the marine fauna in the Thule district (Northwest Greenland) with observations on ice conditions in 1939-41. Meddr. Gronland 150, 54-64.
Wainwright, P. C. and Day, S. W. (2007). The
forces exerted by aquatic suction feeders on their prey. J. R. Soc.
Interface 4,553
-560.
Wainwright, P., Carroll, A. M., Collar, D. C., Day, S. W.,
Higham, T. E. and Holzman, R. A. (2007). Suction feeding
mechanics, performance, and diversity in fishes. Integr. Comp.
Biol. 47,96
-106.
Werth, A. (2000a). A kinematic study of suction feeding and associated behavior in the long-finned pilot whale, Globicephala melas (Traill). Mar. Mamm. Sci. 16,299 -314.[CrossRef]
Werth, A. (2000b). Feeding in marine mammals. In Feeding (ed. K. Schwenk), pp.487 -526. New York: Academic Press.
Werth, A. J. (2006a). Odontocete suction feeding: experimental analysis of water flow and head shape. J. Morphol. 267,1415 -1428.[CrossRef][Medline]
Werth, A. J. (2006b). Mandibular and dental variation and the evolution of suction feeding in Odontoceti. J. Mamm. 87,579 -588.[CrossRef]
Werth, A. J. (2007). Adaptations of the cetacean hyolingual apparatus for aquatic feeding and thermoregulation. Anat. Rec. 290,546 -568.[CrossRef][Medline]
Wilga, C. D., Motta, P. J. and Sanford, C. P.
(2007). Evolution and ecology of feeding in elasmobranches.
Integr. Comp. Biol. 47,55
-69.
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  S. Van Wassenbergh, J. Brecko, P. Aerts, I. Stouten, G. Vanheusden, A. Camps, R. Van Damme, and A. Herrel Hydrodynamic constraints on prey-capture performance in forward-striking snakes J R Soc Interface, October 14, 2009; (2009) rsif.2009.0385v1. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Van Wassenbergh and P. Aerts Aquatic suction feeding dynamics: insights from computational modelling J R Soc Interface, February 6, 2009; 6(31): 149 - 158. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
