~oologicalJournal of the Linnean Society (1986), 88: 277-290. With 5 figures
Functional design of the feeding mechanism
in lower vertebrates: unidirectional and
bidirectional flow systems in the
tiger salamander
GEORGE V. LAUDER* AND H. BRADLEY SHAFFERt
Department of Anatomy and Committee on Evolutionary Biology,
University o f Chicago, 1025 E . 57th Street, Chicago,
Illinois 60637, U.S.A.
Received June 1985, accepted for publication September 1985
There are two basic designs of the aquatic feeding mechanism in lower vertebrates: unidirectional
and bidirectional flow systems. Larval salamanders and most fishes posses a unidirectional flow
design in which water drawn into the mouth with the prey passes over the gills and exits
posteriorly. Metamorphosed salamanders and all other aquatic vertebrates possess a bidirectional
system in which water flows into and out of the mouth during a single feeding cycle. We
investigated the functional consequences of these two feeding designs in larval and metamorphosed
tiger salamanders (Ambystoma tigrinum) feeding in the water. Buccal cavity pressures were measured
during feeding and 1 I variables measured from the pressure traces. Significant differences were
found between the larval and metamorphosed salamanders in eight variables. Larval salamanders
generate significantly greater negative pressures than do metamorphosed individuals and a
principal components analysis of the 1 1 pressure variables completely separates larval from
metamorphosed salamanders. Larval individuals are significantly better at capturing elusive prey
than are metamorphosed salamanders, apparently because of changes in the structure of the feeding
mechanism and the concomitant functional modifications.
KEY WORDS:-Functional
performance.
morphology
-
feeding
-
salamander
metamorphosis
~
-
pressure
CONTENTS
Introduction . . . . . . . .
Material and methods
. . . . .
Experimental animals . . . . .
Experimental techniques . . . .
Data analysis . . . . . . .
Results
. . . . . . . . .
Discussion . . . . . . . . .
Functional morphology
. . . .
Feeding performance . . . . .
Functional design of the vertebrate skull
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278
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28 1
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*Present address: Department of Developmental and Cell Biology, University of California, Irvine,
California 92717, U.S.A.
?Present address: Department of Ecology and Evolution, University of California, Irvine, California 927 17,
U.S.A.
0024-4082/86/110277
+ 14 $03.00/0
277
0 1986 The Linnean Society of London
G. V. LAUDER AND H. B. SHAFFER
278
Acknowledgements
References.
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289
289
INTRODUCTION
There are two fundamental designs of the feeding mechanism in aquatic
vertebrates: unidirectional and bidirectional flow systems. Feeding in the water
involves the creation of a negative pressure in the mouth cavity by movements
of the head and throat, and the pressure differential between the mouth cavity
and the water in front of the mouth results in a flow of water and prey into the
mouth known as suction feeding (Lauder, 1985a). I n unidirectional flow
systems, the water that is drawn into the mouth with the prey passes through
the mouth cavity and exits posteriorly between the gill supports (Lauder,
1985b): flow is from anterior to posterior only. Larval salamanders and most
fishes feed with unidirectional flow, and in such systems the precise timing of
movements of the gill bars, gill rakers and associated soft tissues plays an
important role in preventing water from entering the buccal cavity from behind
the head (Lauder & Shaffer, 1985).
Metamorphosed salamanders and other aquatic tetrapods feeding in the
water utilize a fundamentally different mechanism with bidirectional flow.
Water drawn into the mouth must also exit through the mouth as there are no
posterior gill openings; flow is thus bidirectional.
Despite the broad potential significance of these two hydrodynamic designs
for our understanding of the function and evolution of the vertebrate skull, all
experimental research to date has focused on the unidirectional flow systems of
fishes (Alexander, 1969, 1970; Liem, 1978; Lauder, 1980; Lauder & Clark,
1984) and salamanders (Lauder & Shaffer, 1985), with the sole exception of the
report of Bramble (1973) on the feeding mechanism of turtles.
I n this paper we provide a quantitative experimental evaluation of the
transformation (during ontogeny) between these two fundamental types of
feeding systems in salamanders and discuss the significance of the difference for
feeding biology and vertebrate skull evolution. As an experimental system we
have chosen a single species that changes from a unidirectional to a bidirectional
feeding mechanism within its lifetime: the tiger salamander Ambystoma tigrinum.
By using a single species which shifts feeding mechanisms during ontogeny, we
avoid many of the problems inherent in comparing morphologically and
phylogenetically distinct species to study the consequences of differences in flow
patterns.
During the natural ontogeny of many populations of Ambystoma tigrinum, a
metamorphosis takes place (Shaffer, 1984) in which the head transforms from a
structure with external gills and posterior gill openings to one in which the
external gills are absent and the gill openings seal off laterally and ventrally
(Fig. 1 ) . The resulting water flow patterns during suction feeding in larval and
metamorphosed Ambystoma tigrinum are shown in Fig. 2.
We use the pattern of pressure change within the mouth cavity to analyse the
functional design of unidirectional and bidirectional feeding systems in
salamanders. Pressure changes directly reflect the effect of muscle activity and
skull bone movement on the water (Alexander, 1969; Lauder, 198513; Lauder &
Shaffer, 1985), and provide an excellent overall indicator of changes in feeding
function.
VERTEBRATE FEEDING MECHANISMS
279
30 m m
Figure 1. Metamorphosis in Amhystoma tigrinurn, illustrating three metamorphic stages in individuals
from the same population used in the experiments described in this paper. Note especially the
transformation of the external gill filaments, the reduction in head size, and the closing off of the
posterior gill membrane.
MATERIAL AND METHODS
Experimental animals
Four larval and four metamorphosed tiger salamanders (Ambystoma tigrinurn
mavortium) were chosen from a series obtained near Boulder, Colorado, U .S.A.
The animals were collected as large, premetamorphic larvae and were held for
several months prior to our experiments. All individuals in this population
normally metamorphose except for occasional “cannibal morphs” (Collins &
Holomuzki, 1983) which may retain the larval morphology for life (T. Cocker,
pers. comm.) . The metamorphosed individuals transformed naturally in our
laboratory. The larvae ranged in size (snout-vent length) from 9.1 to 10.2 cm
(mean =9.5; S . D . =0.5), while the metamorphosed individuals ranged from 8.4
to 9.5 cm (mean=8.9; S.D. =0.5). Animals were held in 40 litre glass aquaria,
and metamorphosed individuals were provided with a slightly submerged
platform from which they could breathe and rest. All animals were fed a diet of
chopped earthworms (Lumbricus). For the experiments in which feeding
performance on different prey was assessed, the salamanders were fed live
guppies (Poecilia, 1 cm total length) and waxworms (Galleria, 1 cm total length).
280
G . V. LAUDER AND
H.8. SHAFFER
Figure 2. Schematic diagram illustrating the distinction between unidirectional and bidirectional
feeding systems in Arnlystomo tigrinurn. T h e larval pattern (above) shows how water drawn into the
mouth with the prey passes unidirectionally through the mouth cavity and exits between the gill
supports posteriorly. I n transformed individuals (below),water that enters the mouth with the prey
must reverse course and exit anteriorly through the mouth as the jaws close. This is a bidirectional
feeding system.
Experimental techniques
Pressures within the buccal cavity were recorded using a slight modification of
a previously published protocol (Lauder & Shaffer, 1985). The salamanders were
anaesthetized with buffered tricaine methanesulphonate and a 5 cm length of
flexible polyethylene tubing was passed through a hole in the skull just lateral to
the midline and posterior to the vomer. T h e end of the tube was flanged, pulled
flush with the roof of the mouth, and anchored with a 1 cm sleeve of larger
tubing. A Millar PC-350 catheter-tipped pressure transducer was then passed
through the tubing to within 1 cm of the buccal cavity. This transducer has a
high frequency response (about 10,000 Hz) , and the pressure signals were
amplified and filtered with a Grass P511J preamplifier at a bandwidth of
0.1-1000 Hz.
A total of 125 feedings were used for the statistical analyses of pressure
recordings, 76 from larval animals and 49 from transformed individuals.
VERTEBRATE FEEDING MECHANISMS
28 1
Data analysis
Eight variables were measured from each pressure trace, and three more
variables were derived from these measurements (Fig. 3); the variable names in
Figure 3 will be used throughout this paper. While we anticipated that some of
these measurements would provide redundant information about the pattern of
pressure change, we tried to characterize the pressure curve in a relatively
complete manner, and then used the statistical analyses to provide a
quantitative measure of the extent of redundancy in the data. This approach
was chosen in part because previous research (Shaffer & Lauder, 1985a, b) had
revealed unexpectedly low patterns of intercorrelation among certain functional
variables associated with prey capture in salamanders.
Each pressure trace was converted to digital form using a DAS 12 bit analogto-digital converter (at a sample rate of 1274 Hz), stored on hard discs
associated with an IBM XT microcomputer, and digitized directly on a
Tektronix 4107 graphics terminal. Area measurements, subject to considerable
error if calculated from points chosen along the curve by hand, were calculated
directly from the digital data.
( 3 ) DURNEG
-
( 4 ) DURPOS
b
- A
t
r
-
( 5 ) TTOPOS
v
l
:
\ (7)AREANEG
(9) M B ; M P w N
MAXNEG
*
c
(6)TTONEG
Figure 3. Measurements taken from the buccal pressure trace in larval and metamorphosed
Ambystoma tign'num. Eight variables were measured directly from the pressure trace using a graphics
terminal, and three ratio variables (numbers %l 1) were derived from these measurements. The
variables measured and their definitions are: ( 1 ) MAXNEG, maximum negative pressure from the
baseline; (2) MAXPOS, maximum positive pressure from the baseline; (3) DURNEG, duration of
the negative pressure component of the waveform; (4)DURPOS, duration of the positive pressure
component of the waveform; (5) TTOPOS, time from the baseline crossing between negative and
positive phases to the maximum positive value; (6) TTONEG, time from the start of pressure
decrease to the maximum negative value; (7) AREANEG, area under the negative portion of the
pressure trace (shown in hatching); (8) AREAPOS, area under the positive portion of the pressure
trace (shown in hatching); (9) MPMN, ratio of the maximum positive value to maximum negative
value; (10) DPDN, ratio of the duration of the negative to the duration of the positive components
of the pressure trace; (1 I ) APAN, ratio of the area of the positive to the area of the negative
component of the pressure trace.
G . V. LAUDER AND H. B. SHAFFER
282
To test for significant differences between larval and transformed salamanders
(groups) and for differences among individuals within groups, a nested analysis
ofvariance (ANOVA) was performed (Sokal & Rohlf, 1981) using the statistical
model and procedures previously discussed (Shaffer & Lauder, 1985a). None of
the standard data transformations used to equalize within-group variances had
any effect on the magnitudes of variance component estimates; we therefore
present components based on the untransformed data in Table 2.
We conducted a principal components analysis on the correlation matrix
derived from a log-transformed data set to summarize the major axes of
variation, to provide an indication of redundancy in the variables measured,
and to assess the multivariate differences in feeding between larval and
transformed salamanders.
RESULTS
Sample pressure patterns obtained from larval and transformed salamanders
are shown in Fig. 4, and summary statistics for each individual are presented in
Table 1. Larval and transformed individuals differ significantly in eight of the
11 variables measured from the pressure traces (Table 2). The three variables
for which no differences are found between these groups are the time to
maximum negative pressure (TTONEG), the time to maximum positive
25-
25--
A Larval
B Lorvol
-
0
5-
200
400
C Metamorphosed
0
200
5r-
D Metamorphosed
400
-
-
0
0
-5
-0
1-
-
-
-5 -
-0
200
400
Time (in 0.786 ms)
0
200
400
Time (in 0.786 ms)
Figure 4. A, B, Sample pressure traces obtained from larval Ambystoma ligrinum feeding on worms. C,
D, Sample pressure traces of metamorphosed Ambystoma tigrinurn feeding on worms. Note the
difference in the magnitude of the pressure traces between larval and metamorphosed individuals.
The two larval traces are from the same individual to show variation between feedings; the same is
true of the traces from the metamorphosed individual.
1
15.3 (7.8)
4.7 (1.5)
53.7 (8.1)
262.5 (16.4)
25.8 (20.1)
20.4 (4.9)
485.9 (106.2)
684 (205)
0.32 (0.09)
5.0 (1.2)
1.4 (0.2)
2
27.2 (8.9)
7.1 (2.0)
58.9 (19.3)
256.8 (52.3)
35.0 (17.7)
27.4 (17.0)
797.7 (202.4)
1002 (255)
0.29 (0.08)
4.6 (1.4)
1.3 (0.07)
3
4
19.5 (6.1)
8.1 (1.8)
51.6 (5.3)
209.5 (38.5)
31.7 (19.0)
23.3 (9.0)
710.2 (203.1)
928 (242)
0.4 (0.08)
4.1 (0.9)
1.3 (0.2)
*In mmHg; tin milliseconds (ms); :in mmHg x ms; §dimensionless.
MAXNEG*
25.6 (3.3)
MAXPOS*
8.7 (1.4)
DURNEGt 47.8 (4.8)
DURPOSt 243.0 (36.4)
TTOPOSt
16.3 (13.4)
TTONEGt 20.0 (3.2)
AREANEG: 792.0 (97.0)
AREAPOS: 1098 (140)
MPMNg
0.34 (0.05)
DPDNS
5.1 (1.0)
APANg
1.4 (0.2)
Variable
Larval
21.7 (8.2)
7.1 (2.3)
52.6 (10.8)
244.3 (41.1)
26.2 (18.7)
22.3 (9.5)
686.6 (199.6)
926.7 (261.7)
0.34 (0.09)
4.8 (1.2)
1.4 (0.22)
3.2 (0.6)
3.4 (1.1)
32.0 (3.2)
47.9 (30.9)
11.8 (2.2)
20.1 (4.1)
60.4 (15.4)
84.1 (41.6)
1.1 (0.3)
1.5 (0.9)
1.4 (0.5)
4.2 (1.7)
3.4 (1.7)
32.1 (8.2)
87.7 (26.6)
21.3 (13.6)
17.1 (7.6)
68.3 (26.8)
161.2 (81.8)
0.9 (0.5)
2.9 (1.3)
2.8 (2.2)
5.9 (3.4)
3.4 (1.3)
37.0 (5.9)
63.9 (65.8)
15.8 (6.2)
22.7 (5.5)
110.6 (44.3)
113.5 (82.0)
0.7 (0.2)
1.8 (2.1)
1.1 (0.7)
7
8
4.6 (3.5)
3.1 (0.8)
44.8 (6.1)
87.7 (46.8)
23.2 (20.5)
28.5 (5.4)
100.4 (62.1)
161.4 (102.0)
0.9 (0.3)
2.0 (1.2)
1.8 (1.4)
4.6 (2.7)
3.4 (1.3)
36.3 (8.0)
74.0 (47.1)
18.6 (13.0)
21.7 (7.2)
85.9 (44.7)
134.3 (84.9)
0.85 (0.38)
2.2 (0.23)
1.8 (0.24)
Mean
6
("N=49)
5
Mean
( N = 76)
Metamorphosed
Table 1. Summary statistics (mean (standard deviation)) for the 11 variables measured from the buccal pressure recordings from four larval
and four metamorphosed Ambystoma tigrinum feeding in the water
284
G . V. LAUDER AND H. B. SHAFFER
Table 2. Variance components (in percentages) from a one-way nested
analysis of variance on each of 11 variables measured from the buccal
pressure recordings
Percentage of total variance (do
Among groups
(135)
Variable
MAXNEG
MAXPOS
DURNEG
DURPOS
TTOPOS
TTONEG
AREANEG
AREAPOS
MPMN
DPDN
APAN
*P<0.05, **P<O.Ol
75**
59*
56**
88***
5
0
86**
84**
66**
65**
5
I
Among individuals,
within groups
(6,108)
9***
19***
9***
2**
11*
15**
7***
7***
5**
3*
17**
Among trials,
within individuals
16
22
35
10
84
85
7
9
29
32
78
* * * P < 0.001,
pressure (TTOPOS), and the ratio of the area under the positive portion of the
curve to the area under the negative portion (APAN). Thus, although larval
salamanders generate significantly larger negative and positive pressures than
transformed individuals (Tables 1 & 2), and the duration of these negative and
positive components of the waveform is longer in larvae (Table 1: DURNEG,
DURPOS), the time taken to reach the maximum positive and negative values
does not change. Similarly, even though the negative and positive components
of the pressure waveform are larger in larvae, the ratio of the positive to
negative areas remains constant across metamorphosis (Tables 1 & 2).
Every variable showed significant differences among individuals within
groups (Table 2), indicating that individual salamanders differ considerably in
their feeding behaviour.
The area variables showed very low variance among feedings within
individuals, indicating that each individual generated a consistent pressure from
feeding to feeding. This holds even though the time taken to reach the
maximum pressures varied considerably among feedings.
The correlation matrix (Table 3) and the loadings on the first principal
component (Table 4) show that several variables are highly intercorrelated and
contribute redundant information about variation in the pressures generated
during feeding. I n particular, the AREAPOS, AREANEG, MAXNEG and
DURPOS variables all have high positive intercorrelations. Also, the ratio of
maximum positive to maximum negative pressure, MPMN, shows relatively
high negative correlations with these variables (Table 3 ) . This suite of five
variables all loaded very strongly on the first principal component (Table 4),
emphasizing that they share a common correlation pattern. A plot of each
feeding trial on the first two principal components (Fig. 5 ) shows that the larval
and metamorphosed salamanders form discrete, non-overlapping clusters in
multivariate space. One feeding in each of two metamorphosed individuals (7
and 8 ) approaches the larval pressure pattern, but with these exceptions the two
MAXNEG
MAXPOS
DURNEG
DURPOS
TTOPOS
TTONEG
AREANEG
AREAPOS
MPMN
DPDN
APAN
1.000
0.841
0.534
0.783
0.148
0.074
0.962
0.909
-0.853
0.702
-0.126
1.000
0.323
0.609
0.078
0.0 12
0.820
0.838
-0.436
0.591
0.062
1.000
0.589
0.123
0.587
0.681
0.537
-0.588
0.273
-0.361
1.000
0.225
0.034
0.825
0.918
-0.716
0.938
0.243
1.000
0.062
0.148
0.213
-0.173
0.215
0.156
1.000
0.155
0.014
-0.114
-0.211
-0.360
1.000
0.923
-0.823
0.690
-0.188
0.862
0.206
1.000
--0.705
MAXNEG MAXPOS DURNEG DURPOS TTOPOS TTONEG AREANEG AREAPOS
1.000
-0.607
0.277
MPMN
1.000
0.444
DPDN
1.000
APAN
Table 3. Correlation matrix for the entire set of 11 variables measured from the buccal pressure traces of
larval and metamorphosed Ambystoma tigrinum feeding in the water. Each correlation coefficient is based on
at least 107 feedings
u1
m
N
4
286
G. V . LAUDER AND H. B. SHAFFER
Table 4. Loadings of the first three principal
components from a principal components analysis
of 11 variables measured from buccal pressure
traces of larval and metamorphosed Ambystoma
tigrinum feeding in the water
Variable
AREAPOS
AREANEG
MAXNEG
DURPOS
MPMN
DPDN
MAXPOS
DURNEG
APAN
TTONEG
TTOPOS
Variance explained (yo)
PC 1
PC2
PC3
0.971
0.970
0.953
0.924
--0.827
0.825
0.792
0.644
0.0 14
0.114
0.229
56
0. I78
-0.160
-0.064
0.187
0.225
0.479
0.117
-0.599
0.856
-0.752
0.126
- 0.008
-0.122
-0.177
0.125
0.060
0.057
-0.240
0.2 12
0.278
0.373
0.826
10
19
feeding designs are clearly distinguishable. All of this separation is along the first
component, again emphasizing that larval and transformed salamanders differ
primarily in their ability to generate large pressures and in variables correlated
with that ability.
The efficiency with which larval and metamorphosed salamanders capture
live prey was tested by providing individuals with relatively immobile bottom
prey (waxworms) and with elusive prey (guppies) in separate timed trials. T h e
results for three larvae and two metamorphosed individuals (Table 5) indicate
-2.5
t
-3.01
-3.0 -2.0
I
,
-1.0
0
I
1.0 2.0
PC 2
I
I
3.0 4.0
I
5.0 6
Figure 5. Plot of principal component 1 vs. component 2 to illustrate the separation of larval from
metamorphosed feedings on the basis of 11 variables measured from the buccal pressure trace. The
correlation matrix and factor loadings for this analysis are given in Tables 3 & 4, respectively.
287
VERTEBRATE FEEDING MECHANISMS
Table 5. Comparative feeding performance on worms and fish by larval and
metamorphosed Ambystoma tigrinum feeding in the water (30 min trials per
individual for each prey type)
Fish
Larval ( N = 3 )
Metamorphosed ( N = 2 )
Worms
No. of
strikes
No. of
captures
Success
30
10
33
20
0
0
(Yo)
No. of
strikes
No. of
captures
Success
44
25
41
93
21
84
(%I
that both feeding designs are very efficient at capturing worms on the bottom,
although larvae (93% success rate) may be slightly more efficient than
metamorphosed individuals (84% success rate). However, metamorphosed
animals were unable to capture fish (a 0% success rate) while larvae were
successful 33% of the time.
DISCUSSION
Functional morphology
The major conclusion to emerge from this study is that the morphological
transformation from a unidirectional to a bidirectional feeding design during the
ontogeny of Ambystoma tigrinum (Figs 1 & 2) results in major changes in both the
pattern of pressure generated and in feeding performance on elusive prey such
as fish. Many aspects of the pressure pattern generated during feeding are
different in larval and transformed individuals, with the most significant change
being a decrease after metamorphosis in the area of the negative and positive
components of the pressure waveform.
Most aspects of the change in pressure patterns during ontogeny are
understandable as a consequence of the morphological transformation at
metamorphosis. At this time, the volume inside the buccal cavity decreases, the
head becomes smaller, and there is a reduction in the mass of musculature
associated with the mandibular and hyoid arches of the skull. I t is thus not too
surprising that the pressures generated by transformed individuals are
substantially less than those produced by larvae (Tables 1 & 2) and that the
area under both the positive and negative portions of the waveform decreases.
These changes in the pressure pattern are most likely not directly related to the
change from a unidirectional to a bidirectional flow pattern.
The area under the pressure trace measures the Impulse (integral of force over
a given time interval; Rouse, 1978), and is equal to the change in momentum of
the body to which the force is applied, i.e. the water and prey in aquatic feeding
systems. I n this case, the areas under the positive and negative aspects of the
buccal pressure trace provide a direct indication of the energy the salamander is
putting into the water during feeding. The first principal component of the
multivariate analysis of the pressure variables is primarily a measure of the
energy content of the pressure signal, as the variables loading highest are the
areas of the pressure trace. Because of the high correlation between positive and
288
G. V. LAUDER AND H. B. SHAFFER
negative pressure areas ( r = 0.923) we cannot say which aspect independently
contributes most to the differences between larval and transformed individuals,
although the negative component is the most important in terms of prey capture
mechanics. However, the data clearly indicate that the energy imparted to the
water by the salamander during prey capture decreases dramatically following
metamorphosis.
A second aspect of the results that was anticipated on the basis of the
morphological transformation and models of aquatic feeding in fishes (Lauder,
1985) was the relative increase in the magnitude of the positive pressure pulse:
the value of the MPMN variable is significantly greater in metamorphosed
individuals (Tables 1 & 2). Because the flow of water must reverse direction
within the mouth in metamorphosed salamanders and mouth cavity volume
decreases more rapidly following peak gape (Table I), a larger positive pressure
is predicted as the mouth closes and water is forced back out the mouth. I n
larvae, as the mouth closes, the gill bars at the back of the head are abducting
(increasing buccal volume), and branchial resistance is decreasing, thus
allowing water to flow posteriorly and out of the buccal cavity.
It is important to note that although the predominant flow of water during
feeding of larval ambystomatids is unidirectional, there is probably a small
reverse flow of water from the region posterior to the head just as the mouth
starts to open. As documented elsewhere (Lauder & Shaffer, 1985), in
ambystomatid larvae there is a brief (5-15 ms) delay between the onset of the
pressure decrease within the buccal cavity and the start of gill bar adduction a t
the back of the head to shut off flow into the mouth. This reverse flow is similar
to the reverse flow found in ray-finned fish suction feeding (Lauder, 1980).
Feeding Performance
Although we have emphasized that there are many significant differences
between the pressures generated in larval and metamorphosed ambystomatid
salamanders feeding in the water, it is possible that the pattern of pressure
change in the mouth cavity has little to d o with any measure of feeding ‘success’
or performance (Arnold, 1983, 1986) in predator-prey interactions. While the
biomechanical significance of the functional transformations during ontogeny
certainly leads one to expect that larval and metamorphosed individuals will
differ in their ability to capture prey, such a conclusion is not guaranteed by
demonstrating differences in pressure alone.
Our feeding performance tests using both immobile prey and elusive prey
confirm that the metamorphosed feeding morphology is less effective than the
larval morphology in capturing elusive prey,
Functional design of the vertebrate skull
Given the fundamental nature of the dichotomy between unidirectional and
bidirectional designs of the feeding mechanism in vertebrates, it is somewhat
surprising that more attention has not been paid to the functional significance of
differences between these two systems, and to the morphological bases of the
differences. Given the conservatism of the unidirectional flow system in lower
vertebrates (Lauder, 1985a), the possibility exists that alternative designs are
VERTEBRATE FEEDING MECHANISMS
289
not possible for aquatic feeding mechanisms in vertebrates. Are the functional
demands of capturing an elusive prey of about the same density as the
surrounding medium so rigid that constraints on the feeding mechanism are
large and there are no alternative solutions with equivalent performance to
unidirectional flow designs?
The evidence presented in this paper indicates that, for ambystomatid
salamanders, bidirectional flow systems perform less well than unidirectional
ones for.elusive prey, and this may be generally true of aquatic vertebrates.
Turtles, however, may possess structural modifications that in part avoid
several of the morphological limitations of the bidirectional flow system in
metamorphosed salamanders. As Bramble (1973) and Shafland (1968) have
shown, the oesophagus expands markedly during the strike and appears to act
as a reservoir that stores water entering the mouth when the prey is captured.
An expandable oesophagus may well be an alternative design solution to some
of the hydrodynamic problems faced by aquatic vertebrates feeding in the
water, and allow a morphologically bidirectional flow system to become
functionally unidirectional by greatly delaying in time (and magnitude) the
reverse flow of water out of the mouth until the prey has entered the buccal
cavity and the jaws have closed. The extent to which other organisms may
utilize this modification of the bidirectional flow system remains a key avenue of
future research on the functional design of aquatic feeding mechanisms.
ACKNOWLEDGEMENTS
We thank Tom Cocker for providing the Ambystoma tigrinurn used in this
paper. Catherine Smither and Dojun Yoshikami wrote the computer programs.
We especially thank Julian Humphries and Peter Wainwright for their insightful
comments and discussions throughout the course of this study. This research was
supported by the Block Fund (University of Chicago), NSF PCM-81-21649 to
George Lauder, and an NSF grant to H. B. Shaffer.
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