Feeding kinematics of Kogia and Tursiops (Odontoceti: Cetacea): characterization of suction and ram feeding
Texas A&M University at Galveston, 5007 Avenue U, Galveston, TX 77551, USA
* Author for correspondence (e-mail: marshalc{at}tamug.edu)
Accepted 18 July 2005
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Summary |
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Key words: odontocete feeding, kinematics, RSI, suction, ram, Kogia, Tursiops
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Introduction |
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The underlying mechanics of odontocete feeding have not been systematically
investigated. Although there is a wealth of information on odontocete anatomy,
surprisingly there are far fewer behavioral investigations to test functional
hypotheses based on anatomical studies alone. The derived oral morphology in
some species would appear to physically restrict the feeding mode to
obligatory suction feeding. For example, male strap-toothed beaked whales
Mesoplodon layardii possess a single pair of mandibular teeth that
grow over the maxillae and constrain the jaws beyond a minimal gape that would
make ram-based prey capture difficult
(Heyning and Mead, 1996). The
throat grooves and enlarged hyolingual musculature of ziphiids, physeterids
and kogiids are presumably adaptations for increasing oral volume related to
suction feeding (Clarke et al.,
1968
; Reidenberg and Laitman,
1994
; Heyning and Mead,
1996
; Werth,
2005
). Robust hyolingual musculature is also present in the
short-finned pilot whale Globicephala melas
(Werth, 1992
;
Reidenberg and Laitman, 1994
),
which is the only odontocete for which a kinematic feeding investigation has
validated the use of suction (Werth,
2000
). However, direct pressure measurements from captive P.
phocoena also confirm that this species has the capability to employ
suction (Kastelein et al.,
1997
).
Experimental investigations on the function of odontocete feeding require
the cooperation of captive species. However, many species are not widespread
in captivity, or do not adapt well to captivity. For example, Kogia
(pygmy and dwarf sperm whales) have a poor success rate in captivity
(Sylvestre, 1983). Yet,
kogiids are of particular interest due to their basal phylogenetic position
within Odontoceti and relatively distant evolutionary relationship to
delphinids (Milinkovich et al.,
1994
; Berta and Sumich,
1999
; Geisler and Sanders,
2003
). Their enlarged hyoid apparatus, gular and tongue
musculature, throat grooves and circular oral orifice suggest that
Kogia use suction and that their suction capability could be one of
the best developed among odontocetes
(Caldwell and Caldwell, 1989
;
Reidenberg and Laitman, 1994
).
In addition, kogiids possess those characteristics that are typical of
odontocetes that are thought to use suction. The snout is blunt and the mouth
is short, with reduced dentition; few, if any, teeth are present in the
maxillae. The relatively gracile underslung mandibles contain up to 16 pairs
of fang-like teeth (Handley,
1966
; Ross, 1978
;
Caldwell and Caldwell, 1989
)
that are likely advantageous for retaining squid in the mouth. As in other
potential suction feeding odontocetes, kogiids are primarily teuthophagous
(Pinedo, 1987
;
Aguiar Dos Santos and Haimovici,
2001
; Wang et al.,
2002
).
Recently, we had the rare opportunity to conduct a detailed kinematic
investigation of Kogia feeding behavior using two species that were
kept alive in captivity for more than one year each
(Manire et al., 2004). The
objective of this study was to characterize the feeding performance and
suction capability of Kogia sp. For comparison, we also investigated
the feeding performance of a presumed ram-based feeder, T. truncatus.
Ram and suction are two ends of a feeding continuum frequently studied in
aquatic vertebrates and have been addressed by numerous investigators (e.g.
Lauder, 1985
;
Aerts, 1990
;
Norton and Brainerd, 1993
;
Motta and Wilga, 2001
;
Wainwright, 2001
;
Carroll et al., 2004
).
Anecdotal observations and morphological data suggest that Kogia sp.
and T. truncatus fall on opposite ends of the ram-suction spectrum.
However, such indices have not been applied to odontocetes. Their apparently
divergent feeding behaviors and distant evolutionary relationship within
Odontoceti make Kogia sp. and T. truncatus interesting
candidates for comparative investigations of odontocete feeding
performance.
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Materials and methods |
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Feeding trials
Feeding performance experiments with Kogia were performed during
two, 2-day sessions at fixed 4 h daytime feeding intervals over 3 months.
Trials were conducted in an 8 m wide circular pool maintained at a depth of
1.5 m(Fig. 1A). Subjects were
recorded feeding from a lateral perspective using a Sony Handycam Vision
DCR-TRV900 or DCR-TRV950 (Shinagawa-Ku, Japan) in an Equinox (Portage, MI,
USA) underwater housing. Video footage was recorded at 60 fields
s-1 at a shutter speed of 1/500 s. Kogia sima subjects
were recorded feeding on whole opalescent inshore squid (Loligo
opalescens) that rested loosely in a trainer's hand, mantle towards
subjects, until drawn into the subjects' mouths. To standardize
camera-to-subject distance, the feeder and camera were stationed in 1 m
quadrants placed 1 m apart. Subjects were offered food until they no longer
showed interest. No K. breviceps subjects were in captivity during
the study period. Footage of K. breviceps was provided subsequent to
`Ami's' death and sequences that met the orientation and landmark criteria of
clarity were analyzed.
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Statistics
Normality was calculated with the Shapiro-Wilk normality test
(Z0.05) and variance obtained with Levene's test for equality of
variance (s2
0.05). When both variance and normality
requirements were met, analyses of variance (ANOVA) were performed to
determine significant differences (P
0.05) of kinematic variables
between feeding trials. Posthoc analyses utilized Scheffe's test to
determine which subjects and subject groups were significantly different. If
variance was significant but normality was met, data were analyzed by
independent sample T-tests (P
0.05). Non-parametric data
were analyzed using Mann-Whitney U tests (P
0.05).
Correlation analyses assessed the positive or negative relatedness of RSI,
timing of feeding events and gape and gular displacements. Pearson's
`r' correlation test calculated significant correlations in
parametric data and Spearman's rho test was implemented for non-parametric
data.
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Results |
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Kogia correlation analysis showed a more negative RSI with
decreased time to maximum gape (Spearman's rho; P0.05) and slower
maximum closing gape angle velocity (Spearman's rho; P
0.05). RSI
values decreased in association with increased time to maximum gular
depression (Pearson's `r'; P
0.05) and increased maximum
gular depression (Pearson's `r'; P
0.05). RSI also
decreased with increased time to maximum gular retraction (Pearson's
`r'; P
0.01) and increased maximum gular retraction
(Pearson's `r'; P
0.01). Maximum gular depression
increased with maximum gular retraction (Spearman's rho; P
0.01).
Time to maximum gape increased with larger maximum gape and faster maximum
food velocity (Pearson's `r'; P
0.05).
Tursiops feeding behavior
Tursiops truncatus subjects exhibited feeding behaviors that were
distinct from those of Kogia. Feeding was more locomotory in nature
and subjects approached frozen herring from at least 3-4 m away. Some
fluctuations in gape and gular movement were noted immediately prior to
feeding. Pectoral fins were frequently flared or rotated outward with the
lateral surface of the flipper faced forward (pronation), presumably as an
effort to slow forward progress within centimeters of food items. Mandibular
depression was slow and gular depression was extensive relative to
Kogia. Gular depression and retraction were not limited to the gular
depression phase and were observed in jaw opening and jaw closing phases
(Fig. 4B,C). Two distinct
ram-based feeding patterns were identified: Tursiops open gape
approach and Tursiops closed gape approach
(Fig. 3C-F). Subjects
performing Tursiops open gape approach feeding behavior entered the
camera's view having 50% of maximum gape or more. Gape increased slowly to
maximum while the subject swam to and captured the food item, at which time
the jaws closed. Tursiops closed gape approach was utilized by both
subjects, but Tursiops open gape approach was utilized only by
`Clicker.' Subjects performing Tursiops closed gape approach feeding
behavior entered the first video field at or near closed gape (<3 cm gape);
a preparatory phase was observed before the jaws rapidly opened to maximum
gape within centimeters of food. Gular depression and retraction and tongue
retraction were visible in most sequences.
Tursiops feeding kinematics
Pooled Tursiops, open gape approach and closed gape approach
feeding variables are summarized in Table
1. Four feeding phases (preparatory, jaw opening, gular depression
and jaw closing) were identified (Fig.
4B,C). Phase I began when maxillary and mandibular tips were
identified; gape was 25% greater than minimum gape. The mean maximum gape
angle, mean maximum opening gape angle velocity, mean maximum gape and mean
time to maximum gape occurred in phase II. Mean maximum closing gape angle
velocity occurred in phase IV. Tursiops closed gape approach feeding
behavior was more representative of the pooled data while Tursiops
open gape approach feeding behavior was more divergent. Phase I was observed
in only one of 11 Tursiops open gape approach feeding sequences, and
the only trial in which tongue retraction was observed measured 1.31 cm and
time to maximum tongue retraction was 300 ms.
Pooled Tursiops correlation analysis showed an increased maximum
gape angle with both increased maximum opening and closing gape angle
velocities (Pearson's `r'; P0.01). Tursiops open gape
approach correlations included increased maximum closing gape angle velocity
with increased maximum opening gape angle velocities (Spearman's rho;
P
0.05). Maximum gape angle increased with both maximum opening
and closing gape angle velocity (Pearson's `r'; P
0.01).
Maximum gular depression increased with increased maximum gular retraction
(Spearman's rho; P
0.01). Within Tursiops closed gape
approach feeding mode, increased RSI correlated with decreased feeding cycle
duration (Spearman's rho; P
0.01) and decreased time to maximum
gular depression (Spearman's rho; P
0.05). Maximum closing gape
angle velocity increased with maximum opening gape angle velocity (Pearson's
`r'; P
0.01). Maximum gape angle increased with both
increased maximum opening and increased closing gape angle velocity (Pearson's
`r'; P
0.01).
Comparative Odontocete kinematics
Kogia and pooled Tursiops
Numerous significant differences were demonstrated between genera. Mean
Kogia RSI values were significantly less than for any
Tursiops group (pooled, open gape or closed gape trials;
P<0.001). Kogia suction distances were greater than for
any Tursiops group (P<0.05)
(Table 2) and Kogia
ram distances were less than any Tursiops group
(P<0.001). The mean total feeding cycle and jaw opening durations
(phase II) were significantly shorter in Kogia than any
Tursiops group (P0.002). Mean gular depression (phase
III) duration was significantly longer in Kogia than
Tursiops open gape approach (P<0.01). Mean maximum gape
angle was greater in Kogia than any Tursiops group
(P
0.005). Mean maximum opening and closing gape angle velocities
were significantly faster in Kogia compared to any Tursiops
group (P<0.01). Mean maximum gape was significantly smaller in
Kogia than any Tursiops group (P<0.01). Mean
time to maximum gape was shorter in Kogia compared to any
Tursiops group (P
0.002). Mean maximum gular depression
was less in Kogia compared to pooled Tursiops and
Tursiops open gape approach (P<0.05). Mean time to
maximum gular depression was significantly faster in Kogia than any
Tursiops group (P<0.05).
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Tursiops open and closed gape approach feeding
Numerous significant differences were also demonstrated between
Tursiops feeding modes. The mean ram distance of Tursiops
open gape approach was significantly greater than pooled Tursiops and
Tursiops closed gape approach (P0.005). Mean feeding
cycle duration with Tursiops open gape approach was longer than the
pooled Tursiops or Tursiops closed gape approach
(P<0.02). The mean jaw opening duration was also longer for
Tursiops open gape approach than for pooled Tursiops
(P<0.02) and Tursiops closed gape approach
(P<0.001). The mean gular depression (phase III) duration was
significantly longer in Tursiops open gape approach than
Tursiops closed gape approach (P<0.01). Mean maximum
opening gape angle velocity was significantly slower in Tursiops open
gape approach compared to pooled Tursiops (P=0.012) and
Tursiops closed gape approach (P<0.001). Mean time to
maximum gape was also significantly longer in Tursiops open gape
approach than pooled Tursiops or Tursiops closed gape
approach (P<0.05). Mean maximum gular retraction was significantly
greater in Tursiops open gape approach compared to Tursiops
closed gape approach (P<0.05).
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Discussion |
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The negative RSI values for Kogia were likely generated by the
simultaneous depression and retraction of the hyoid apparatus, which in turn
would have depressed and retracted the tongue. The rapidity of this movement,
relative to Tursiops, would likely have produced negative intraoral
pressures, and analysis of feeding trial footage verifies that suction is
produced (food moved into the mouth). In addition, suction production was also
likely influenced by the rapid increase in gape and gape angle relative to
Tursiops. In general, the kinematic profile of Kogia
resembles that of Tursiops closed gape approach
(Fig. 4A,B), except for overall
shorter durations of events. This rapidity of motion was likely significant in
the development of intraoral pressures. The fact that Kogia gular
depression and retraction were not as extensive as Tursiops is likely
a scaling factor and not related to the relative magnitude of suction
produced. Kogia subjects possessed a mandible that was largely
recessed within the confines of the head, and only the distal one-third of the
mandible was external compared to two-thirds for Tursiops. This
resulted in a larger gape in Tursiops compared to Kogia.
However, gape angle was greater in Kogia vs Tursiops, and this wide
gape angle is probably one of the greatest of any odontocete, with the
possible exception of Physeter
(Werth, 2005). The short
external mandible, in conjunction with the specialized ridges of tissue on the
lateral perimeter of the mandible, served to occlude the lateral gape of the
jaw and helped produce a tubular mouth opening; a surprising adaptation in an
odontocete. Other marine mammals, such as walruses Odobenus rosmarus
(Kastelein et al., 1991
) and
belugas Delphinapterus leucas
(Brodie, 1989
), use elaborated
orofacial musculature to occlude this region. Several throat grooves present
in the gular region of K. sima may have assisted in allowing greater
depression and retraction of the gular region.
Kogia feeding must allow for the expulsion of water following food capture. Kogia subjects generally maintained a partial gape subsequent to phase IV, probably to allow water to exit. When Kogia subjects retained food after a feeding event, squid were often held in the mouth by the elongated mandibular teeth with the mouth still partially open. It appeared that only a light pressure was applied to retain food and it was doubtful that a soft-bodied cephalopod could significantly encumber gape closure. Furthermore, more forceful jaw closure could hinder squid removal from the teeth. The opposite behavior to suction is the forceful jetting of water out of the mouth, or hydraulic jetting. Hydraulic jetting was observed in 25% of Kogia feeding trials and could be influential in the capture of benthic prey or in manipulation of prey.
Two major caveats of the Kogia data were that subjects were young
and that feeding trials ended prematurely due to the death of both subjects.
This event was not unexpected since kogiids have a poor success rate in
captivity (Sylvestre, 1983).
The situation in this study was unique in that these subjects survived for
more than one year (Manire et al.,
2004
). Kogia subjects were less than one year old, at
least partially dependent upon formula diets and did not swallow food in any
recorded session. It is possible that sucking behavior could have been derived
from suckling, as in other mammals (Gordon
and Herring, 1987
; German et
al., 1992
; Thexton et al.,
1998
), and is not completely representative of feeding in adult
Kogia. Without more definitive techniques such as cineradiography and
pressure transducer measurements to assess tongue movement and its affect on
intraoral pressures (as used by Thexton et
al., 2004
), the precise mechanism of odontocete suction generation
remains unclear. However, the K. breviceps subject had consumed whole
squid for the last 15 of 21 months of captivity. Food was routinely
manipulated and introduced into the mouth by both subjects. Only events that
mimicked feeding were analyzed; manipulatory behaviors were eliminated from
analyses. Due to their young age and inexperience, feeding behavior by
Kogia subjects was likely uncoordinated. However, significant suction
events were still recorded despite the subjects' inexperience. Further study
of older kogiids may show an even stronger suction capability than reported in
this study.
The rapid feeding cycle of Kogia is consistent with kinematic data
from pilot whales G. melas. Werth
(2000) also found a four-phase
feeding cycle in G. melas that is unlike the feeding cycle of
terrestrial mammals (Hiiemae and Crompton,
1985
), but likely derived from it. The mean Kogia feeding
cycle duration was approximately 100 ms shorter than that of G. melas
and 10-179 ms shorter in all phases except jaw closing (phase IV), where
G. melas was 120 ms shorter. The more rapid Kogia feeding
cycle suggests a greater suction capability than G. melas and this is
supported by hyolingual data for both species
(Reidenberg and Laitman,
1994
). Once food had entered the oral cavity, greater water
expulsion may have slowed Kogia jaw closure. A longer Kogia
jaw closing phase duration than with G. melas may also have resulted
from an ability of Kogia to retain food by their elongated teeth,
which would not require the more rapid gape closure seen in G.
melas.
Kinematics of ram-based feeding
Tursiops RSI values were distinctly ram-based, with little, if
any, suction component to feeding. Effective suction occurs over a limited
distance and changes in RSI values result primarily from modulation of ram
distance (Wainwright, 2001). The greater ram distances of Tursiops
relative to Kogia are responsible for the greater RSI values of
Tursiops and support a more locomotory feeding strategy for
Tursiops in this study. Suction distance means
(Table 2) likewise support a
lesser degree of suction feeding in Tursiops, as food items
frequently moved away from subjects, potentially due to bow waves formed at
the rostral maxillae and mandibular tips of Tursiops subjects. A
small Tursiops suction component may have been present to help reduce
the affect of this positive pressure wave. Although a significant suction
feeding component was not observed here, Tursiops is known to
participate in a variety of feeding modes under different conditions and a
significant suction component may be present under different conditions.
Tursiops gape kinematics were distinct from Kogia. The relatively slower gape velocities, time to maximum gape and jaw opening (phase II) durations of Tursiops likely resulted in more positive RSI values. The observation that maximum closing gape angle velocity was generally faster than maximum opening gape angle velocity in Tursiops was likely because of the need to capture food items once within reach and would be expected for a ram-based feeder.
As in Kogia, Tursiops gular movement occurred over most of the feeding cycle and was not limited to the gular depression phase. Forward motion of Tursiops was essential in food capture. In several cases, numerous capelin Mallotus villosus were simultaneously offered to Tursiops subjects. Gape and gular movements alone were insufficient to draw food items into the mouth and in several trials successful food capture did not involve any gular depression or retraction. This was a key behavioral difference between Kogia and Tursiops.
The function(s) of pectoral flares is unclear, but may increase the
accuracy of capture attempts or reduce bow wave pressure formed on the rostral
tip, which could minimize food being pushed away or allow for a suction
component in the final moment before capture. In either case, pectoral flares
may be an important feeding modulation in free-ranging Tursiops
attempting to capture elusive prey. In this study, flares appeared to slow
forward motion in Tursiops subjects when in close proximity to food,
from about 50 cm s-1 to near 0 cm s-1. Although observed
in most feeding sequences, flares did not always occur and may have been in
response to the enclosed environment in which subjects were located. Pectoral
pronation was similarly observed in a kinematic analysis of pilot whales
(Werth, 2000) to slow forward
motion in the final stages of food approach.
Tursiops open and closed gape approaches were different from each other, but were both strongly ram-based. The slowly increasing gape of Tursiops open gape approach resulted in all significant differences of gape and feeding duration variables between Tursiops open and closed gape approaches. Gular depression and retraction were observed even when a large partial gape was present. A preparatory phase was observed in only one of 11 trials of Tursiops open gape approach behavior and was not included in the kinematic profile of Tursiops open gape approach feeding (Fig. 4C). However, it is likely that a preparatory phase was always present in Tursiops open gape approach, but occurred before the subject entered the video camera's field of view. Early gape may serve to reduce response time for capture of more elusive prey.
In summary, broad morphological differences between Kogia and Tursiops are reflected in their different feeding performances. Kogia was observed to feed primarily using suction, which likely relied upon rapid gape and gular kinematics to produce negative intraoral pressures and draw food into the mouth. Tursiops was primarily ram-based, exhibited slower gape and gular kinematics and always overtook food by locomotion. The Tursiops feeding repertoire in this study included two distinct feeding patterns that were dissimilar in the timing of gape increase. Kinematic data support the functional hypothesis that odontocetes can produce suction by the rapid depression and retraction of the hyolingual apparatus, but also demonstrate that rapid jaw opening and wide gape may serve to increase suction capability. Furthermore, these data serve to provide a foundation for future kinematic studies that can place odontocete feeding biomechanics within an evolutionary perspective.
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Acknowledgments |
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