AMER. ZOOL., 29:65-84 (1989)
Locomotion in Amphibian Larvae
(or "Why Aren't Tadpoles Built Like Fishes?")1
RICHARD J. WASSERSUG
Department of Anatomy, Dalhousie University, Halifax, \'ova Scotia B3H 4H7, Canada
SYNOPSIS. A variety of morphological features that affect locomotion distinguish larvae
of the three living amphibian orders from fishes and their larvae. The oddest amphibian
larvae are anuran tadpoles. With their globose bodies, concealed forelimbs, abruptly
compressed and terminally tapered tails, tadpoles not only differ radically fromfishesbut
they—unlike caecilians or salamanders—also differ radically from their adults. Tadpoles
typically have less axial musculature and much simpler myotomes than fishes. Surprisingly,
in terms of mechanical (propeller) efficiency and maximum sprint speeds, tadpoles still
perform as well as many teleosts of comparable sizes. From a consideration of hydromechanics, no amphibian larvae appear to be designed for sustained swimming at high
speeds. High maneuverability, rather than sustainable speed, are important for amphibian
larval survival.
Two key features of tadpoles are the absence of caudal vertebrae and unexposed pectoral
appendages. With only a notochord to serve as a skeleton, the tadpole tail is extremely
flexible. Because of this exceptional flexibility, tadpoles can fold their tails up against the
body and turn rapidly with virtually no displacement of their center of mass. Caudal
flexibility can be regulated by muscle activity in the tadpole to effect turning. Lateral
appendages are not needed for this movement and are free to develop directly into their
adult morphology; the anterior ones develop under cover of an opercular fold where they
do not contribute to drag. A case is presented, based on the ecology of metamorphosis,
that anuran transformation should be as brief as possible. With no bone to resorb, metamorphosis of the anuran caudal appendage can, indeed, be very rapid.
The basic kinematics of constant velocity straightforward swimming for tadpoles and
salamander larvae is reviewed, as well as the kinematics and electromyography of starting,
stopping, and turning in tadpoles. An attempt is made to relate swimming kinematics to
the characteristic morphologies of amphibian larvae. Swimming speed in Rana, Bufo and
Aynbystoma larvae, which swim only intermittently, is modulated by changing tail beat
frequency. However, Xenopus, which swims constantly by sculling with its tail, regulates
swimming speed (at low to intermediate velocities) by varying the length of the propulsive
wave in its tail. Xenopus and Rana differ in the morphology of their notochord, spinal
cord, spinal nerves, and spinal motor pool distribution within the spinal cord. These
differences may underlie the different way these larvae regulate swimming. They may
also reflect their phylogenetic history.
that the locomotion of anuran larvae is dieb v t n e n e e d o f
these organisms to
undergo rapid metamorphosis,
M
y approach is a comparative one.
Unfortunately, so little is known about
either the morphology or behavior for one
order, the Gymnophiona, that they may be
d e a l t w i t h vei
7 briefly, as follows,
Caecilians are limbless, largely fossorial,
vermiform amphibians. Adults of one familv a n d larvae in t w o
others are aquatic,
Larvae and adults of the most observed
species with aquatic larvae, Ichthyophis kohtaoensis, behave similarly in the water. They
will swim with their snouts out of the water
and can move both backward and forward
• From the Sympos.um on Axial Movement System:
•
controlled fashion (Crapon de CaBwmechanics and Neural Control presented at the
JTTJ ino=\ A • u u
Annual Meeting of the American Society of Zoolo- prona and Himstedt, 1985). At night t h e
gists, 27-30 December 1986, at Nashville, Tennessee, larvae crawl among rocks under water in
INTRODUCTION
Aquatic larvae occur in all three orders
of living amphibians: salamanders (Caudata), frogs (Anura) and caecilians (Gymnophiona). A variety of morphological features that affect locomotion distinguish
these amphibian larvae from fishes and
their larvae. In this essay I examine the
basic kinematics of swimming in amphibian larvae and contrast it to that of fishes,
I examine how the locomotor behavior of
amphibian larvae is imposed by their morphology. In particular, I explore the notion
65
tated
66
RICHARD J. WASSERSUG
search of food; during the day they hide
several centimeters deep among the same
rocks. The greatest gross morphological
difference between Ichthyophis larvae and
adults that could affect aquatic locomotion
is the presence of a small, medial fin fold
around the end of the body in the larvae.
This is lost at metamorphosis (Breckenridge et al., 1987). The extreme elongation
of both adult and larval caecilians, in comparison to most other amphibians, is best
interpreted as an adaptation for fossorial
existence (Gans, 1975).
Somewhat more is known about the
locomotion of urodele larvae and these data
will be summarized in the following
account. However, my main focus will be
on tadpoles—anuran larvae—because
these organisms offer the most difficult
challenge to understanding the relationship between morphology and locomotor
behavior. Whereas no amphibian larvae
look quite like fishes, salamander and caecilian larvae at least look like their respective adults. The locomotor system of these
non-anuran larvae changes relatively little
with growth and metamorphosis. Gills and
fleshy tail fins are resorbed, but no major
appendages are lost or abruptly appear.
One may reasonably suppose that most of
the larval morphology of these organisms
reflects the locomotor needs of the developing adult whether terrestrial or aquatic.
In contrast, tadpoles with their globose,
seemingly inflexible head/body, long
tapered tail, covered forelimbs and hidden
gills look like neither adult frogs nor the
larvae of other vertebrates. By understanding the kinematic implications of their
unique morphology one may gain some
insight into the relation between morphology and swimming behavior of other
aquatic organisms.
WHY AREN'T TADPOLES
BUILT LIKE FISHES?
Defining the problem
Tadpoles have been presumed to swim
in an "ineffective and uncontrolled" manner compared to modern fishes (Romer,
1966, p. 22). Such a presumption is not
unreasonable on strictly anatomical
grounds. Because their bodies do not taper
gracefully into their tails, tadpoles simply
do not look as streamlined as most fishes.
Tadpoles lack pectoral and pelvic fins. They
lack erectile axial fins. Their terminally
pointed, rather than expanded, tail is the
antithesis of what one expects from an efficient caudal propeller on hydromechanical
grounds (Weihs, 1988). No adult vertebrates have axial musculature more simply
arranged than the parallel-fibered, chevron-shaped myotomes of tadpoles (cf. fig.
1 in Bone, 1978). The maximum percentage of total mass devoted to the axial musculoskeletal system in any tadpole is 45%
(for large, i.e., 8-9 cm, Xenopus just before
metamorphosis), but for most tadpoles this
value is less than 30% (Hoffand Wassersug,
1986). Carangiform and subcarangiform
fishes, by comparison, may have up to twice
the amount of propulsive musculature
(Aleyev, 1977): muscle mass for dace (Leuciscus leuciscus, 6-10 cm) range from 4 7 61% of total mass (Bainbridge, 1960) and
for several larger scombrid species from
56 to 68% (Fierstine and Walters, 1968,
with the proportion of muscle mass scaling
as approximately the third power of length;
Wardle, 1977; Graham etal, 1983). In sum,
considering their rotund bodies, their lack
of lateral or erectile fins, and how much
less locomotor musculature tadpoles have
to work with, it seems unlikely that their
locomotor performance and control could
match that of most teleost groups.
Only during the last decade have there
been any quantitative data on swimming in
anuran larvae that address the question of
their locomotor effectiveness. Whereas
these data refute the overly simplistic classification of these organisms as "ineffective
and uncontrolled," one aspect of tadpole
locomotion that clearly gives the impression of being inefficient is that they tend
to show substantial lateral oscillation, or
recoil, at the snout (Wassersug and Hoff,
1985). This, however, is a kinematic feature that they share with larval fishes
(Rosenthal, 1968; Batty, 1981, 1984). In
fact, for their sizes, tadpoles compare quite
favorably to teleosts in a variety of ways.
Tadpoles, for example, can swim as fast as
teleost fishes of comparable sizes, at least
over short distances (see Table 1; compare
67
LOCOMOTION IN AMPHIBIAN LARVAE
with table 4 in Beamish, 1978 andfig.6-2
in Yates, 1983). Maximum sprint speeds,
and tail beat frequencies at given swimming speeds for tadpoles match those
reported for fishes of comparable sizes
(Wassersug and Hoff, 1985), although not
necessarily tested under exactly the same
conditions. Feder (1983) has shown that
tadpoles often outswim natural predators,
such as turtles, when engaged in a chase.
Nor is the ability of tadpoles to turn
handicapped by the absence of lateral
appendages. Videotapes of mature larvae
of both Rana pipiens and Xenopus laevis indicate that they can rotate through 180°, with
little or no translation, in approximately
30 msec (at 20°C). Films reveal that this is
accomplished with a C-start that differs little from the C-start of fishes (as defined by
Webb, 1986a and earlier workers), except
that tadpoles can completely fold their
bodies on their tails. Because of their great
caudal flexibility (vide infra "Locomotion
and Metamorphosis"), tadpoles can bring
the sides of their bodies into contact with
their tails. They effectively pivot in place
about their center of mass by a two-part
action. First, they fold (adduct) their heads
toward their tails, then they unfold (abduct)
their tails away from their bodies (see for
example, fig. 11 in Blight, 1977; fig. 1 in
Rocketal., 1981). Anguilliform fishes have
comparable flexibility allowing them to
bring their heads into direct contact with
their bodies (see for example,fig.3 in Eaton
and Hackett, 1984), but it is not known
whether they can use this action to pivot
in place with the same speed as tadpoles.
What can fishes do that tadpoles can't?
Many fishes, particularly carangiform and
thunniform fishes with lunate tails, can sustain high speeds in open water whereas no
tadpoles do so, and based on data on stamina (Wassersug and Feder, 1983), it is
unlikely that any could. It is probably in
terms of maximal sustainable velocity that
the relatively slight axial musculature, high
axial flexibility, and tail shape of tadpoles
cost them the most in performance. From
a consideration of hydromechanics (Weihs,
1988), tadpoles are not well designed for
energetically efficient locomotion at high
speeds. Even at a modest cruising speed of
TABLE 1. Maximum sprint speeds maintained for 3 or
more lengths, and tail beatfrequenciesfor anuran larvae. *
Rana catesbeiana
Rana sylvatica
Rana septentrionalis
Bufo americanus
Xenopus leavis
Specific
swimming
speed
(lengths sec-)
Absolute
speed
(cm sec"1)
Tail beat
frequency
(sec")
23
22
29
24
19
92
86
116
90
76
28
32
32
31
28
* All tadpoles were 3.75-4.0 cm in total length and
tested at 21 ± 1°C. Raw data from tadpoles filmed at
>200 frames s e c ' ; courtesy of K. v. S. Hoff.
2-4 lengths sec"1, the distance travelled
per tail beat as a fraction of total length
(i.e., stride length) is 20 to 25% less for
tadpoles (Rana) than for sturgeon (Acipenser) or trout (Salmo) (fig. 4 in Webb, 1986b).
In other words, tadpoles must beat their
tails faster and accelerate water to relatively higher velocity to achieve the same
speed as these actinopterygian fishes.
I have never observed tadpoles swimming for long periods at any appreciable
velocity. (Although some long endurance
records were obtained for tadpoles in flow
tank studies by Wassersug and Feder
[1983], those data do not apply to natural
situations because the larvae were allowed
intermittent stops.) Open water chases of
tadpoles by turtles rarely last more than a
dozen seconds before the turtle either
catches the tadpole or loses the trail (Feder,
1983). Brief periods (<1 min) of vigorous
activity by tadpoles are typically followed
by a period of immobility (Werschkul and
Christensen, 1977; Caldwell et al, 1980).
Gatten etal. (1984) have demonstrated that
it takes only 30 sec of intense activity to
deplete completely the phosphocreatine
reserves of Hyla or Rana tadpoles. They
concluded that for tadpoles "successful
avoidance of a predator depends on rapid
changes in direction . . . and apparently on
the velocity or acceleration but not on the
endurance of the swimming . . . ." (In this
connection it is worth noting that most tadpoles are cryptically colored and live close
to cover; few live out in the open in large
bodies of water [Loschenkohl, 1986]). The
high tail fins of tadpoles provide them with
large lateral surfaces and that is the profile
68
RICHARD J. WASSERSUG
one expects in undulatory swimmers
designed for transient swimming (acceleration and turning) rather than cruising
(Webb, 1984; Webb and Blake, 1985;
Weihs, 1988). The axial musculature of
tadpoles, in the few species that have been
examined, is almost all white muscle, with
red fibers restricted to a thin subcutaneous
shell (Horiguchi and Watanabe, 1984;
Kordylewski, 1986; Hoff, 1987).
In addition to their ability to sustain high
speeds, most fishes have lateral appendages
that allow midwater postural displays.
These include all the intricate pectoral and
pelvic fin movements used by fishes in agonistic, territorial and mating behavior.
These behaviors are absent from the
anuran larval repertoire; inter- and intraspecific postural displays are simply not
known in tadpoles (although larger tadpoles will push smaller conspecifics away
from food; Savage, 1961). The ability of
anuran larvae to hover is limited to those
forms with well-developed lungs and filamentous tails. How amphibian larvae regulate buoyancy is not fully understood, but
it involves open lungs rather than a closed
gas bladder with a rete mirabile. A specialized organ for buoyancy regulation may
give fishes some advantage in fine postural
control (Gee, 1983).
Although fishes may have some advantages over anuran larvae in maximum sustainable speed and in fine midwater movements, tadpoles can do one thing that fishes
cannot; they can change quickly into a radically different sort of organism. No fishes
are known to go through as extensive and
at the same time as rapid a morphological
transformation as anurans at metamorphosis. I would like to explore the thesis that
features of swimming ability and rapid
metamorphosis trade off against each other;
viz. a need to metamorphose rapidly may
account for why tadpoles are not built like
fishes.
Locomotion and metamorphosis
Before trying to relate locomotor design
to metamorphosis, a comment is necessary
on what it means, in an ecological sense,
to be a tadpole. There is substantial field
work demonstrating the massive impact
that the feeding activity of tadpoles can
have on primary aquatic productivity
(Seale, 1980). This has fostered a view of
tadpoles as "feeding machines," which
delay maturation of their reproductive
organs (definitional to being "larval") in
favor of morphological structures for
ingestion and digestion (Wassersug, 1975,
1980). Anatomically, tadpoles are little
more than mouth, guts and tail, and for
their size can, indeed, ingest an enormous
amount of food over a very short time
(Wassersug, 1972; Seale and Wassersug,
1979; Seale et al., 1982). Fifty percent of
the total mass of a tadpole may be gastrointestinal contents alone (Calef, 1973).
This morphological focus on feeding, at
the temporary expense of other organ systems, is a good design in aquatic habitats
when primary productivity is exceptionally
high but predators are few. Such environments are the temporary rain pools, ditches
and vernal ponds that tadpoles characteristically inhabit. These small bodies of water
may be nutrient-rich during part of the
year, and tadpoles can grow very quickly
in them. However, from a tadpole's perspective, such habitats deteriorate quickly.
Either inter- or intraspecific competitors
lower the amount of available food (Morin,
1983; Smith, 1983), or increasing predation—from invertebrates within the ponds
and vertebrates both within and around
the pond—takes its toll on the tadpoles
(e.g., Cronin and Travis, 1986; Formanowicz, 1986). Or, the ponds simply dry up.
Therefore tadpoles, which make use of this
rich but temporary resource, require a
mechanism of escaping from their ponds
when the probability of mortality rises and/
or their growth rates decline (Werner,
1986). Metamorphosis is essential. There
are no anurans that breed as larvae; all
must metamorphose.
At metamorphosis a tadpole goes from
a singular reliance on undulatory, axial
locomotion to an equally singular reliance
on saltatory, appendicular locomotion (see
Stehouwer and Farel [1985] for an introduction to the neurobiology of this transformation). Metamorphosis, however, is a
LOCOMOTION IN AMPHIBIAN LARVAE
relatively dangerous stage in the life cycle
of anurans, and this returns us to the issue
of locomotion. Tadpoles in the middle of
metamorphosis, with forelimbs exposed but
the tail still present, can neither sustain
their position in a water current as long as
developmentally less advanced siblings, nor
hop as far on land as developmentally more
advanced siblings, with their tails already
regressed (Wassersug and Sperry, 1977).
These locomotor differences are ecologically meaningful in that predators capture
individual anurans in the middle of metamorphosis significantly more often than
they capture either premetamorphic tadpoles in the water or fully transformed
young on land. Arnold and Wassersug
(1978), in turn, demonstrated with snake
stomach content analyses that the disproportionately high vulnerability of metamorphosing anurans to predation in the
laboratory was true in the wild. They concluded that natural selection, through predation, has acted to make anuran metamorphic climax as brief a period as possible
in the life cycle of the anuran.
I believe that most of the unique features
of the tadpole locomotor system relate to
this need to undergo metamorphosis as
quickly as possible. Two striking examples
are the concealed forelimbs and a simplified caudal skeleton. In this section I introduce these morphological features and in
the following sections explore their effects
on tadpole swimming.
Part of the uniqueness of the tadpole is
that its forelimbs develop completely covered by an opercular fold. The forelimbs
are not necessary for turning (vide infra
"How do Amphibian Larvae Start, Stop
and Turn?") and could only contribute to
drag in a fashion disadvantageous to steady
swimming. On the other hand, functional
forelimbs are essential for the anuran the
moment it completes metamorphosis (Wassersug and Sperry, 1977); for in order to
jump effectively, a newly transformed
anuran must be able to extend its forelimbs
and elevate its head approximately 45°. To
meet this demand, the tadpole develops
fully functional adult forelimbs within the
confines of its larval body. Here the fore-
69
limbs do not penalize steady swimming, but
neither do they enhance maneuverability;
braking and turning must be accomplished
entirely by axial mechanisms.
A second morphological feature, significant to an hypothesized trade-off between
larval locomotion and rapid metamorphosis, is that anuran larvae do not have any
vertebrae in their tails (Fig. 1). Although
there may be as many as three post-sacral
vertebral elements depending on the
species (Branham and List, 1979) that will
ultimately form the adult urostyle, these
elements do not extend into the tadpole
tail proper despite the etymology of the
word "urostyle" (Mahendra, 1956). The
only caudal skeletal element in the anuran
larva is the notochord. If bone were present in the tail, resorption would necessarily
be slower since the catabolic breakdown of
denser, hard tissues is slower than that of
soft tissues.
The mechanical implication of a tail
without vertebrae is that flexibility is
increased, at the expense of stiffness. The
mechanical role of a stiff axial skeleton for
fishes is clear when one examines models
for the generation of thrust during acceleration and drag during turning and braking (see for example, Aleyev, 1977; various
papers in Webb and Weihs, 1983; Hess and
Videler, 1984; Videler, 1985; Webb,
1986a; Weihs, 1988). Fishes, in addition to
having caudal vertebrae, have fin rays in
their medial and lateral fins that stiffen
these propulsive surfaces. It is not a coincidence that fin rays and vertebrae are
among the earliest elements to ossify in fish
ontogeny (see various articles and figs, in
Lasker, 1981 and Moser et ai, 1984).
Other elements that stiffen the tails of
fishes are also absent in tadpoles; scales, for
example. Tadpole myotomes are not the
inter-nested complex type of fishes (cf.
Horiguchi and Watanabe [ 1984] plus older
papers by Watanabe et al. and Sasaki cited
therein, for tadpoles; Alexander [1969] and
Wainwright [1983] for fishes). Tadpoles
lack the complex myotomal septation of
fishes. Tadpoles, likefishes,do have crossed
collagen fiber wrapping in their tail fins,
as has been reported by several workers
RICHARD J. WASSERSUG
FIG. 1. Cleared and stained larvae of the anuran Rana catesbeiana (above) and the salamander Ambystoma
tigrinum (below). The specimens were stained for both cartilage and bone. They are of approximately the
same size and developmental stage. Note the complete absence of a caudal skeleton in the tadpole compared
to the well developed caudal skeleton in the salamander larva.
(e.g., Weber, 1961; Overton, 1976; Warren, 1981). But since the caudal musculature does not extend into the fins, it is
doubtful that skin and underlying connective tissue could act as an "external tendon" in quite the way proposed for fishes
(see Hebrank and Hebrank, 1986, plus
papers cited therein). Tadpole skin is relatively delicate and highly vascularized,
which is of some importance given the
major role in respiration played by the skin
in these organisms (Feder and Burggren,
1985). In sum, a number of factors contribute to the decreased stiffness of the tadpole tail relative to that of fishes. Of these,
probably the most important is the absence
of tail vertebrae. This decreased stiffness
limits the amount of potential energy that
the tail can store as it is bent and contributes significantly to the characteristic kinematic profile of swimming tadpoles.
In the following sections I review in
greater detail what is known about the
kinematics of swimming for both tadpoles
and salamander larvae. I identify ways in
which the kinematics of amphibian larvae
is both similar to and different from that
of fishes, and suggest how the differences
may be dictated by morphology. The situation in which acceleration is zero is
treated first, followed by an examination
of what is known about swimming where
linear and angular acceleration are not
zero.
SUMMARY OF BASIC KINEMATICS FOR
CONSTANT VELOCITY SWIMMING IN
AMPHIBIAN LARVAE
The following comments apply to swimming in a straight path at constant velocity
for larval Ambystoma (A. maculatum and
mexicanum), which are just beginning to be
studied, and for the Rana (R. catesbeiana,
syliatica, septentrionalis, rlamitan1;) and Bufo
LOCOMOTION IN AMPHIBIAN LARVAE
20
15
freq
u
a>
Tail
s
10 -
">^^
5
ft
0
o
.30
oc
=^
.25
/
^
§.—
.15
Maxiimum
at tip
ific
lil
.20 .
.10
.05
B
-'
0
•
•
•
•
•
•
i
1 2
ngtti
re (I
1.0
•
0.8
a> %
0.6
peciti
propi
io -s2
0.4
CO
0.2
0
•
c
•
.
.
i
.
71
(B. americanus) tadpoles examined by Wassersug and Hoff (1985). Given their conservative morphology, the kinematic patterns reported here for Rana and Bufo are
likely to hold for other bottom-dwelling
anuran larvae of similar gross proportions.
The midwater Xenopus larva is considered
separately because of its rather different
behavior, gross morphology, and neuronal
organization.
Figure 2 schematically summarizes the
basic relationship between swimming speed
and four kinematic variables for tadpoles:
tail beat frequency, maximum amplitude
(lateral movement away from the path of
forward motion) of the propulsive wave in
the tail, maximum length of the propulsive
wave, and Froude efficiency, a standard
measure of mechanical efficiency (see
Webb, 1975). The dependent variable,
speed, is given as "specific swimming
speed," in units of total lengths-sec"1, which
allows for convenient comparisons among
animals of different sizes.
As amphibian larvae swim at higher
speeds, they increase tail beat frequency in
a linear fashion (Fig. 2A). The correlation
between these variables is highly significant for tadpoles, such as Bufo and Rana,
and for the salamander Ambystoma (see
Table 2 plus unpublished data). The slope
for the tadpole regression line falls very
close to the mean slope for this relationship
0.9
0.8
0.7
0.6
4
8
12
Specific swimming speed, (Ls-1)
FIG. 2. Summary kinematics for tadpoles swimming
at constant velocities along straight paths. Solid lines
represent Rana and Bufo; dashed lines represent Xenopus; based on data from Wassersug and Hoff(1985)
and Hoff and Wassersug (1986). The variance in
amplitude among species of Rana is great and thus
two lines are given in B. The upper line is for shorttailed forms and the lower line is for longer tailed
forms. Although the scatter about the lines is not
shown, all lines, with the exception of the horizontal
segments in C, are statistically significant at P < 0.05
or better. A general conclusion that can be drawn
from this figure is that tadpole kinematics is fundamentally similar to that of subcarangiform fishes
(Bainbridge, 1958; Webb, 1975).
The major differences between Xenopus, which sculls
continuously with the terminal portion of its tail, and
the other tadpoles is that at low velocities (<6 lengthssec"1) Xenopus regulates swimming speed by varying
the length of the propulsive wave in its tail (C) and
not its tail beat frequency (A). Also, as indicated by
the longer, descending line segment in D, Xenopus can
swim at lower speeds (with lower efficiencies) than the
other larvae while at the highest speeds it has high
efficiencies. On the other hand, the maximum velocity recorded to date for Xenopus falls below that of
other tadpoles (see Table 1).
72
RICHARD J. WASSERSUG
for fishes almost exactly (compare Fig. 2D
with Webb, 1975).
Where tadpole kinematics diverges most
from that of fishes is in the function and
control of the portion of their tail that is
caudal to the high point of the tail fin; the
terminal segment. With each half of a tail
beat the terminal segment of the tail in
tadpoles crosses the path of forward motion
at an angle of approximately 90° from that
path (Wassersug and Hoff, 1985). At such
a high angle of incidence (Fig. 3) the tail
tip cannot actively contribute to thrust and,
we suggested, is more likely dragged passively.
We then demonstrated that the norFIG. 3. Tracings from single film frames of Bufo
americanus and Ambysloma maculatum swimming at a mal wave form for the posterior tail of free
constant velocity of 3.5 cmsec" 1 . Films were taken at swimming tadpoles could be completely
200 frames-sec"'. The tadpole is shown here at the reproduced in anaesthetized tadpoles simend of a single tail beat cycle. Note that its tail tip is ply by passively oscillating them. Not surmoving forward as the tadpole moves forward. Such
behavior by this segment of the tail suggests that it prisingly, the middle portion of the tail, at
could not be providing thrust and probably is pas- the point where the tail fin is highest, had
sively dragged by the tadpole (see Fig. 4). Note the an angle of incidence close to 0° as that
high amplitude and wave form for the propulsive wave body segment crossed the path of forward
in the salamander larva. Unlike the tadpole, curvature motion. The kinematic profile for this porin the trunk is conspicuous and substantial.
tion of the tail (Fig. 4) is most appropriate
for the maximum generation of thrust in
reported for a large variety of teleost fishes the additive mass mode of Weihs (1988).
(data summarized in Wassersug and Hoff,
The terminal segment of the tail, never1985). At low speeds the maximum ampli- theless, has a positive influence on locotude of the propulsive wave, which occurs motion even though it may not contribute
at the tip of the tail, is low. However, it directly to thrust. This was demonstrated
rapidly increases asymptotically to a max- conclusively by amputating the tail tip in
imum value in the neighborhood of 0.25 both freely swimming and anaesthetized
lengths with increasing speed (Fig. 2B). The tadpoles mounted on a mechanical oscilsame curve and asymptote were obtained lator (Wassersug and Hoff, 1985). Tests
for fishes (Bainbridge, 1958).
with streams of dye revealed that the terData accumulated so far do not reveal a minal portion of the tail reduces turbustrong relationship between the length of lence behind the tadpole. The tapered, terthe propulsive wave and swimming speed minal segment acts as ballast influencing
for most amphibian larvae (Fig. 2C). For the amplitude of the tail further forward
tadpoles with longer tails (e.g., Rana septen- where the tail fin is the highest and thrust
trionalis and R. clamitans), wavelength can be optimally produced. Specifically, the
increases somewhat with increased speed tapered posterior portion of the tail—even
(Wassersug and Hoff, 1985). Wavelength when it is passively dragged behind the tadcorrelates more strongly with size. As with pole—dampens the lateral excursion of the
tadpoles, some fishes demonstrate a posi- midtail and keeps the angle of incidence
tive relationship between velocity and pro- for that portion of the tail low. Two lines
pulsive wavelength while others show no of evidence support this conclusion. First,
relationship (Webb, 19866). The lowest as can be seen in Figure 2B, tadpoles with
Froude efficiencies recorded are approxi- longer tails have lower relative amplitudes.
mately 0.6. Froude efficiency rises rapidly Secondly, and more conclusively, when a
as swimming speed increases, then levels tadpole tail is surgically truncated to
off at just above 0.8 (Fig. 2D). The tadpole resemble that of most teleost fishes, amplidata fit the curve relating these variables tude and the concomitant angle of inci-
73
L O C O M O T I O N IN A M P H I B I A N L A R V A E
TAIL TIP
Maximum
MIDTAIL
FIG. 4. A schematic drawing comparing the kinematics of the terminal segment of the tail with the midtail
for a representative Rana or Bufo tadpole swimming on a straight path, at a constant velocity in the neighborhood of 2-4 lengths sec"1. (Taken from Wassersug and Hoff, 1985.)
The horizontal axes represent the mean path of forward motion for the whole animal. Three kinematic
parameters are overlain on each graph. They are: the position of each body segment with respect to the path
of forward motion (=the path traced out in space by that segment as the tadpole moves forward); the angle
of incidence, which is the angle that a tangent to that segment makes with the path of forward motion; and
the lateral velocity of that segment (i.e., its velocity perpendicular to the path of forward motion) plotted
through time. The vertical axes are standardized so that both velocity and angle of incidence are plotted as
a proportion of maximum, normalized to 1.0. The band widths indicate the range of variation seen in the
raw data.
Note that when the tail tip crosses the path of forward motion, its lateral velocity may be high, but its angle
of incidence is also high (sometimes exceeding 90°). Thus, it could impart little momentum posteriorly and
contribute little thrust for forward progress. Overall variation is high. In contrast, as the midtail approaches
the path of forward motion its velocity increases and the angle of incidence decreases. The variance is reduced
compared to that of the tail tip. Water is displaced posteriorly so that this portion of the tail contributes
effectively to forward propulsion.
dence for the midtail of both free swimming tadpoles and anaesthetized tadpoles
on the oscillator rises well above optimum
values. (Optimum angle of incidence for
subcarangiform fishes is considered to be
in the neighborhood of ±10°; Videler and
Wardle, 1978).
These observations give us insight into
why the tadpole tail is tapered rather than
truncated, or even expanded in lunate-like
fashion behind a caudal peduncle, as it is
in so many fishes. In fish with a lunate tail
the intrinsic stiffness of the peduncle and
the tail limit the amplitude of the caudal
fin. In tadpoles, however, where terminal
mass rather than rigidity limits amplitude,
the angle of incidence is such that the tail
will progressively contribute more to drag
and less to thrust as one retreats caudally
from the midtail. To reduce this drag, the
74
RICHARD J. WASSERSUG
surface area of the tail should become progressively diminished as one moves further
caudally. This, of course, is exactly what
one sees. In the absence of skeletal elements to stiffen the tail, the tadpole tail
should and does taper to a point.
Not only does the tail bend during swimming, but there is evidence of lateral bending in the vertebral column within the trunk
of tadpoles during normal swimming,
despite their short vertebral column and
globose, seemingly inflexible bodies. Neurophysiological data indicate alternating
ipsilateral/contralateral waves of motor
activity in the trunk region of Rana larvae
during fictive swimming (Stehouwer and
Farel, 1980). Approximately half of the
axial muscle mass in typical pond tadpoles
lies in the trunk, and it would be surprising
if unilateral firing of this much muscle did
not deflect the vertebral column. Stehouwer has further pointed out (personal communication) how data on amplitude at various points along the body for a R.
catesbeiana swimming at 2.4 lengths-sec"1
(in Wassersug and Hoff, 1985) indicate that
the vertebral column is, in fact, bending.
The crucial observation is that amplitude
is higher at the snout than at the base of
the tail even though the snout is closer to
the point of rotation where amplitude is
effectively zero, i.e., the midpoint between
the otic capsules. This could only be possible if some lateral bending is taking place.
The zygopophyseal facets on tadpole vertebrae are in the frontal plane and would
permit this motion. Manipulation of cleared
and stained specimens confirms that some
lateral flexion is possible without subluxation of the vertebrae.2
The kinematic differences between salamander larvae and tadpoles are mostly in
the wave form and pattern of amplitude
2
Whereas the trunk bends during swimming in
amphibian larvae, both salamanders and anurans have,
as a potential counter-measure, a mechanism for
reducing lateral flexion at the base of the tail. Both
frog and salamander larvae extend their exposed limbs
and adpress them (and, in the case of salamanders,
their gills as well) against their body when swimming
at higher speeds. D. Stehouwer (personal communication) has suggested that the hindlimbs in this situation may stiffen the base of the tail as they embrace
it.
for the propulsive wave (Fig. 3). In tadpoles
the point of least amplitude is at the back
of the cranium, specifically between the otic
capsules. This is the part of the body with
the smallest change in acceleration through
each tail beat cycle. Tadpoles oscillate about
that point, which means that their inner
ears—their accelerometers—move forward on a stable base. In salamanders the
point of lowest amplitude on the body is
often posterior to the otic capsules. At low
speeds this point is near the head, but as
swimming speed increases the lateral
excursions of the snout increase and the
point of lowest amplitude moves progressively caudal. Amplitude at the tail tip is
also higher in Ambystoma than in tadpoles
at comparable speeds (Table 2). In this
regard, the Ambystoma larva resembles
closely the classic kinematic profiles provided by Gray (1933) for eels and for eellike herring larvae by Batty (1984). Blight
(1977) also noted the similarity in these
high amplitude lateral movements in the
swimming of salamander larvae (Triturus
helveticus) and eel-like aquatic chordates,
although he did not contrast either with
tadpoles. Amphibian larvae collectively
have been said to swim in the anguilliform
(eel) mode (Lighthill, 1975) and although
there are several definitions for the
"anguilliform mode" in the literature (see
Lindsey, 1978; Braun and Reif, 1985;
Webb and Blake, 1985), the statement
appears to be strictly and narrowly correct,
at least for salamanders and caecilians. For
Ambystoma larvae the length of the propulsive wave is often less than the length
of the animal, whereas for Rana and Bufo
the wavelength is usually greater than the
length of the animal. In this regard tadpole
swimming is more similar to that of subcarangiform fishes.
Blight (1977) suggested two patterns of
motor activity associated with waves of
bending in swimming vertebrates. In the
first, which he called "resistance-dominated," waves of bending are driven by
waves of rostral to caudal muscle contraction. In the second, which he called "stiffness-dominated," muscles on one side are
fired simultaneously and not serially, yet
waves of bending are still propagated in a
whip-like fashion because of the decreasing
75
LOCOMOTION IN AMPHIBIAN LARVAE
TABLE 2. Summary kinematics for constant velocity swimming by larval salamanders compared to tadpoles.
Species
L
(cm)
Tail beat
Velocity, U
freAbsolute Specific quency
(cm sec"1) (L sec"1)
Max
Min
Max
Specific
\elocit)
of the
propulsive
wa\e, V
(L-sec-)
0.81
1.27
0.89
0.80
0.9
0.13
0.06
0.05
0.37
0.45
0.31
0.29
6.3
4.4
6.5
5.9
0.53
0.79
0.47
0.52
0.77
0.89
0.74
0.76
1.86
0.05
0.20
6J)
0.50
0.75
0.08
0.32
5.8
0.56
0.78
0.03-0.04
0.14-0.27
6.2
0.52
0.76
0.0
0.14
6.4
0.50
0.75
Amplitude ui pnjjjuiM\c wave
Absolute (cm)
Specific (L)
Mm
Ambystoma maculatum
Specimen
3.4
# 1
2.2
7.4
8.7
0.20
3.5 11.1 0.36
#2* a
2.8
9.8
0.17
b
2.8
8.7
7.7
3.1
3.1
0.14
#3
2.8
8.7
6.3
Ambystoma mexicanum
7.7
0.42
(one specimen) 9.1 27.3
3J)
Some averages for comparison
3.2
8.3
with anurans**
Values for Rana and Bufo larvae (taken from Wassersug
and Hoff, 1985) swimming
3.2
6.7
at the same specific velocity
Values for Xenopus larvae (taken from HofF and Wassersug, 1986) swimming at the
3.2
9.8
same specific velocity
* Two separate swimming sequences.
** All anurans between 1 and 6 cm in length.
stiffness down the rostral-caudal axis (see
also Videler, 1985). Blight (1977) presented EMG data for larvae of the European newt Triturus helveticus that showed
both patterns: at low swimming speeds
there are rostral to caudal lags in ipsilateral
EMG records, while at higher speeds these
lags disappear.
Electrophysiological work with tadpoles
reveals these same two patterns (Stehouwer and Farel, 1980; Hoff, 1987). Hoff has
demonstrated that Rana catesbeiana larvae
have two preferred swimming speeds and
tail beat frequencies. The actual speeds and
frequencies are, in part, size dependent as
has been reported for fishes (Webb, 1977);
i.e., smaller fishes and tadpoles have higher
tail beat frequencies at their preferred
swimming speed. When unstressed, 10 cm
bullfrog tadpoles at room temperature
preferred to swim slowly at approximately
3 tail beats per second. Here, a distinct
rostral-caudal lag was picked up by the
EMG electrodes, indicating that the
myotomes were active in series. Under
these conditions Hoff found no muscle
activity in the terminal portion of the tail,
as predicted (Wassersug and Hoff, 1985).
Mechanical
effici lency
Froude
Slip
(17= 1 -
(L'A)
0.5(1 L/V)
However, when stimulated mechanically by
prodding, the same bullfrog tadpoles preferred a tail beat frequency closer to
10-sec"1. Then the rostral-caudal lag in
ipsilateral muscle contraction disappeared,
indicating simultaneous muscle contraction. In this situation, EMG activity was
found at least as far caudally as 80% of total
length. Taken together, these results provide evidence that amphibian larvae exhibit
two distinct neuromuscular patterns for the
regulation of simple undulatory movement
in the absence of any acceleration. Unfortunately they do not, however, address the
emerging question of how the central nervous system and structural properties of
the tail interact to determine the preferred
swimming speed(s) of any species and the
switch from one neuromuscular control
pattern to the other.
How Do AMPHIBIAN LARVAE START,
STOP AND TURN?
Starting and stopping
Webb (1986a) and others distinguish a
single C-start from an S-start in fishes. For
predaceous fishes striking at prey, the
S-configuration allows for the control of
76
RICHARD J. WASSERSUG
recoil. Lateral forces cancel each other out,
and the predator is able to propel itself
forward with its head aimed directly at its
prey. T h e single C-start, in contrast,
advances a fish forward along a path at
some greater than zero angle of deviation
from its original orientation. Thus, a C-start
involves some amount of turning and, as
the amount of turning is often unpredictable to an observer, it is the C-start that
should, and does, serve fishes best during
flight from predators (Weihs and Webb,
1984).
The same two behaviors have been noted
for amphibian larvae under similar circumstances. Salamander larvae in the water
column use an S-start to strike at prey (Hoff
et al., 1985). There are a few species of
anurans with predaceous tadpoles, but
because of their relatively inflexible torso
and short tails these tadpoles do not achieve
the wholebody S-configuration of predaceous fishes and salamanders. Consistent
with this, no predaceous tadpoles are
known to make extended high velocity
strikes and chases. None, for instance,
overswim their prey with their mouths
open; i.e., none are "ram feeders," following the terminology of Liem (1980).
Instead, to keep their mouths on target and
catch prey, predaceous tadpoles must either
scull slowly with their tails to get close
enough to suck prey into their mouths (e.g.,
as does the pipid Hymenochirus, personal
observation), or wait until prey make the
error of coming too close to them. Basically, predaceous tadpoles capture prey by
the same inertial suction mechanism used
by their more generalized, suspensionfeeding relatives (Wassersug and HofF,
1979; Ruibal and Thomas, 1988).
Both salamander larvae and tadpoles
exhibit the C-configuration during fast
starts to escape predators, but not all movements by amphibian larvae, of course, are
initiated as fast starts. A tight C, for example, is not observed when amphibian larvae
begin swimming at low speeds. Rather, the
C-start has been associated traditionally
with a startle response. In this situation all
of the muscles on one side of the body
should fire simultaneously to maximize
thrust (Blight, 1977), while those on the
contralateral side are silent. Electromyography data confirm simultaneous activity
of both rostral and caudal ipsilateral
myotomes during C-starts (Hoff, 1987). In
the startle response of fishes, the inhibition
of motor activity on the extended side of
the vertebral column is often, but not
always, Mauthner cell mediated (see Eaton
and Hackett, 1984; Eaton et al., 1984; Nissanov and Eaton, 1988). Most amphibian
larvae have Mauthner's neurons that could
mediate their fast starts (Rocked a/., 1981).
Bufo tadpoles supposedly lack Mauthner's
neurons (Stefanelli, 1951; Moulton et al.,
1968; but see Hughes, 1959, p. 137) yet
still show a C-start startle response and,
surprisingly, can quickly accelerate to
velocities nearly as high as the highest
recorded so far for comparably sized ranids
or hylids (Table 1, plus data summarized
in fig. 16 of Wassersug and HofF, 1985).
Thus, as in fishes, Mauthner's neurons may
not be essential for amphibian fast starts.
Amphibian larvae can stop their forward
motion by a variety of methods. Salamanders extend lateral appendages, which
include not only limbs, but external gills
(HofF et al, 1985). They may also hook
their tails to increase frontal area and drag.
Tadpoles occasionally hook their tails, but
this is not common and was, in fact, rarely
observed on our films. More commonly
tadpoles stop simply by ceasing to swim.
Tadpoles are small enough and swim at low
enough absolute velocities that the hydrodynamics of intermediate Reynolds numbers (Re < 5 x 10") apply (Vogel, 1981).
Here viscous forces are not inconsequential and a tadpole which ceases active swimming glides to a halt in a short distance,
usually less than 2 lengths. Essentially, tadpoles need not actively brake. They are of
low enough mass that they can afford to
glide to a halt even if it occasionally means
hitting an obstacle. When fleeing a predator a tadpole can run headlong into vegetation and under cover; its momentum is
so low that it is unlikely to sustain injury.
Braking by hooking the tail increases frontal pressure drag and, consequently,
increases turbulence which may stir up sediment and can signal the presence of a tadpole to the visual, electro- and mechanical
LOCOMOTION IN AMPHIBIAN LARVAE
receptors of potential predators. A tadpole
is far less conspicuous if it keeps flow around
it laminar. It is, in fact, not uncommon for
tadpoles, when disturbed in nature, to swim
at high velocity into mud or bottom vegetation and to disappear into the substrate
with little trace of their point of entry.
Hoff (1987) has coined the term"I-stop"
for the straight-tailed, gliding stop of tadpoles, as opposed to a "J-stop" where the
tail is hooked. Her EMGs unexpectedly
reveal that the I-stop is an active behavior
involving isometric motor activity. In an
I-stop, muscles in the anterior portion of
the tail are silent, but the posterior ones
show prolonged simultaneous activity on
both sides. As a result the caudal portion
of the tail stiffens, dampening out oscillation.
As already noted, the only alternative to
the gliding I-stop for tadpoles is to brake
with a J-stop, but in the absence of paired
lateral appendages, anuran larvae cannot
execute this braking maneuver without
turning. (This is another kinematic feature
which distinguishes them from fishes with
lateral appendages.) This may not seem like
a particularly elegant way to stop, but from
an ecological perspective it is certainly adequate and may even have advantages over
a gliding stop. If a tadpole is swimming
toward a recognized hazard, such as an
attacking predator, stopping will not
increase its chances of survival. Rather what
is important is that it change direction. It
is the turning, not the stopping, which is
crucial.
Turning
Fishes initiate turning by using their lateral appendages asymmetrically to induce
drag and lift asymmetrically. This role for
lateral appendages is so well established that
it is easy to assume that lateral appendages
are essential for turning by aquatic vertebrates. This is, of course, not correct for
tadpoles, and certain fishes, most notably
agnathans, turn perfectly well without
them. The kinetics and neuromuscular
control of this action are not fully understood.
Let us first consider the simplest case of
turning in the horizontal plane. The small
77
amount of axial musculature (< 10% of total
weight) in the tail of pond tadpoles posterior to the high point of their tail fin is
important in such movements (Wassersug
and Hoff, 1985). Hoff (1987) has verified
this with EMGs of free swimming tadpoles.
Whereas the posterior myotomes are electrically inactive when tadpoles are swimming in a straight line at average speeds
(with waves of bending propagated passively in the terminal portion of the tail),
those same posterior myotomes fire as soon
as a tadpole starts to turn.
As myotomes contract they, in theory,
affect turning in two ways, both of which
seem to occur in tadpoles to varying degrees
depending on the radius of curvature and
speed of the turn (Hoff, 1987). First and
most obviously, small asymmetries in either
the intensity or timing of otherwise normal
alternating waves of muscle contraction will
deflect the tail to one side, altering the
mean direction of thrust. Secondly, antagonistic muscle activity can vary the stiffness
of the tail. All else being equal, if the tail
tip is stifFer as it moves toward the path of
forward motion from one side than from
the other, momentum will be transferred
asymmetrically to the water. This can turn
the tadpole, but it requires that stiffness be
altered within half of a tail beat cycle. This
mechanism is most likely to be used in the
situation where the propulsive wave proper
is primarily generated more anteriorly in
the tail. By either actively bending the end
of the tail more to one side or the other,
or by stiffening the tail during only one
part of the tail beat cycle, the tadpole turns.
Both mechanisms may be at play concurrently. Essentially this is the same distinction made by Blight (1977) in his discussion
of "resistance-dominated" vs. "stiffnessdominated" waves of bending, applied
regionally and asymmetrically within the
tail. Hoff (1987) has presented EMG data
to confirm that both of these alternative
neuromuscular patterns are involved in
turning by tadpoles.
Since most fishes have osseous rays within
their caudal fin maintaining a relatively
fixed stiffness, rather than muscle there to
vary stiffness, they cannot alter the stiffness
of this terminal appendage extensively to
78
RICHARD J. WASSERSUG
effect a turn (however, see Lauder, 1988).
Presumably this is why so many of them
utilize, instead, lateral appendages in turning. Salamander larvae extend their lateral
appendages asymmetrically when striking
at prey not directly in front of them (Hoff
et ai, 1985). Thus they, like fishes, use pectoral and pelvic structures for turning. To
what extent they also use axial methods of
turning, like tadpoles, is not known.
Because caecilians lack lateral appendages
they only use axial muscles for turning.
As noted above, the tadpole's sole reliance for turning on its highly, but variably
flexible muscular tail—instead of on lateral appendages—means that it can
develop directly its adult forelimbs within
the confines of its body, where they will
not contribute to drag. Through this line
of reasoning, the tadpole's unique floppy
tail and equally unique opercular fold may
be considered part of a single functional
complex that permits effective larval locomotion, and at the same time facilitates fast
metamorphosis.
Our discussion of turning so far has been
limited to movements in the horizontal
plane. Amphibian larvae can also ascend
and descend rapidly. Salamanders presumably use lateral appendages as well as movements of their trunk proper during vertical
turning. Many aquatic salamanders and
caecilians have a dorsoventrally flattened
head—simple flexion and extension in the
cervical and trunk region should help them
turn up or down. I know, though, of no
kinematic analyses of these movements.
Tadpoles can turn vertically without lateral appendages or releasing air from their
lungs. Lungless tadpoles move up and down
as well as lunged tadpoles so the behavior
does not depend on buoyancy regulation
via changing air sac volume. Few tadpoles
appear capable of flexing or extending their
head on their torso, like salamanders might,
to assist in turning in the vertical plane (but
see discussion of the shovel-snouted, fossorial Otophryne robusta larva for an exception; Wassersug and Pyburn, 1987). Affleck
(1950, p. 359) asserts that the tadpole "tail
is flexible in the vertical plane" and that
"the animal is able to initiate upward or
downward movements by flexing the tail
upward or downward." I know of no evidence to support this. Preliminary observations in my laboratory of tadpoles surfacing to breathe air suggest that rapid
vertical movements require rolling which,
in turn, requires torsion in the tail. The
most obvious mechanism for applying
torque to the tail is differential contraction
of epaxial and hypaxial portions of caudal
muscle chevrons. Electromyography could,
conceivably, confirm whether this is,
indeed, how it is done.
SWIMMING IN XENOPUS
LARVAE—FREQUENCY VERSUS
WAVELENGTH REGULATION AND ITS
POSSIBLE MORPHOLOGICAL CORRELATES
Tadpoles of most genera are negatively
buoyant, swim only intermittently, and
when they are not actively moving they
sink to the bottom. Xenopus larvae (and
those of a few other genera, notably in the
family Microhylidae and the hylid genera
Hyla, Phyllomedusa and Agalychnis), in con-
trast, live midwater and never rest on the
bottom. Rather they swim continuously by
rapidly vibrating the filamentous terminus
of their tails. Xenopus tadpoles are positively buoyant and scull, in a head down
position, against their own buoyancy.
Movement in the Xenopus tail is normally
confined to the end of the tail. There are
no waves of bending visible in the tail anteriorly, except when the tadpole swims fast
(>6 lengths-sec"1).
Not only do Xenopus larvae differ from
other tadpoles in terms of where they swim,
how often they swim, and what part of the
tail they use to propel themselves, but they
differ fundamentally in the way that they
regulate their speed during basic straightforward, constant velocity swimming (Fig.
2). Rana and Bufo tadpoles, as noted earlier, change velocity by changing tail beat
frequency (Fig. 2A), while the length of
the propulsive wave changes little (Fig. 2C).
This is consistent with the idea that constant structural properties of the tail—for
example, the ridigity of the notochord—
rather than local muscle activity determine
how that portion of the tail deforms. Xen-
LOCOMOTION IN AMPHIBIAN LARVAE
opus, on the other hand, maintains a constant tail beat frequency over a broad range
of swimming velocities and increases speed
by increasing the length of the propulsive
wave (Fig. 2C). Waves of bending in the
posterior tail are, thus, under direct, local
myotomal control. As Xenopus larvae swim
faster they incorporate more and more of
their tail in the power stroke. Only for
velocities above approximately 6 lengthssec"1, where the length of the propulsive
wave is so long that the whole tail is undulating, must Xenopus increase tail beat frequency, like other tadpoles, in order to
swim any faster (Fig. 2A).
What underlies these kinematic differences? Regrettably, despite an enormous
amount of neurobiological research on
locomotor control mechanisms in Rana and
Xenopus, parallel studies have not been done
on similarly staged animals. Most of the
work on Xenopus, in fact, has been done on
embryos (e.g., summarized in Roberts el ai,
1983; Roberts, 1988) rather than tadpoles,
and Xenopus embryos do not swim like
mature larvae.
Nishikawa et al. (1985) and Nishikawa
and Wassersug (1985, 1988) have documented major differences in the gross morphology of the spinal cord in Rana vs. Xenopus larvae. The Rana larval cord narrows
abruptly in the sacral region and is reduced
caudally to a filum terminale made up of
little more than an ependymal tube. Axons
to myotomes beyond the 10th post-sacral
segment travel through a caudal plexus
instead of through the spinal cord (Brown,
1946). In Xenopus, in contrast, the spinal
cord is larger throughout the tail, and
paired spinal nerves exit the cord in oneto-one correspondence with the caudal
myotomes for more than 20 post-sacral
body segments. Horseradish peroxidase
studies (Nishikawa and Wassersug, 1988)
show that motoneurons for caudal
myotomes in Rana lie far forward in the
lumbar spinal cord whereas those of Xenopus lie near the myotomes in the caudal
spinal cord proper. These differences are
remarkable: the Rana larval pattern is similar to that of adult frogs, or for that matter
mammals, with a short spinal cord and a
79
cauda equina; the larval Xenopus pattern is
like that of tailed lower vertebrates, such
as salamanders and lizards (Nieuwenhuys,
1964).
It is intriguing to think that the differences in spinal cord morphology relate to
the differences in the use of the tail and in
the regulation of swimming between Rana
and Xenopus. This may, in part, be true.
The Xenopus pattern, in theory, would allow
for absolutely shorter reflex loops to the
more caudal myotomes than in Rana. However, gross spinal cord morphology similar
to that of Xenopus larvae occurs in other
anurans, such as discoglossoid larvae
(Nishikawa and Wassersug, 1985, 1989),
which neither live midwater nor scull with
the ends of their tails. There is, thus, some
suggestion that there are phylogenetic as
well as functional influences on the neuronal patterns of locomotor control in tadpoles.
A note on the notochord
Anuran larvae have a specialized caudal
notochord compared to that of other vertebrates (Leeson and Threadgold, 1960).
The elastic layers of the notochordal sheath
are particularly thick, presumably storing
and releasing elastic strain (potential
energy) with each half tail beat. The notochord in Rana tigrina (Mahendra, 1956)
and tadpoles of other species (personal
observation) is laterally compressed, with
a recess dorsally for the spinal cord and
one ventrally for the caudal artery. This
shape suggests that the tadpole notochord
may have taken on some of the protective
functions served elsewhere in the vertebrate world by the osseous and cartilaginous elements of the axial skeleton.
As discussed earlier, the tapered terminal portion of a Rana tadpole's tail is electromyographically silent during normal,
straightforward swimming at moderate
speeds (Hoff, 1987). Unlike the rest of the
tail, the terminal portion functions more
to reduce turbulence than to generate
thrust (Wassersug and Hoff, 1985). In this
regard, it is noteworthy that the notochordal sheath, in Rana catesbeiana at least,
changes abruptly just posterior to the high
80
RICHARD J. WASSERSUG
point of the tail fin (Bruns and Gross, 1970).
Anterior to that point, the elastic layer lies
superficial to the notochordal sheath, and
distally it lies deep to the sheath. The exact
biomechanical implication of this change
is not known, but it is consistent with a shift
in function between the anterior and posterior portions of the tail.
Xenopus, in contrast, has no similar rostral-caudal shift in notochordal structure
(Khajeh Dalooi, 1977). This is consistent
with the fact that Xenopus uses a continuously variable portion of the tail to generate thrust (starting from back to front),
depending on swimming speed. Thus, differences in the kinematics and regulation
of swimming between Rana and Xenopus
are reflected not only in the central nervous system but also in the notochord. The
specializations of the notochord of anuran
larvae in general, and the variation between
these genera, emphasize the importance of
tissues other than nerve and muscle on the
caudal mechanics of amphibian larvae.
CONCLUSIONS AND SUMMARY
For the study of pure axial locomotion,
anuran larvae would, at first glance, appear
to be nearly ideal model organisms. Until
metamorphosis, anterior appendages are
not exposed outside of the body wall and
contribute to neither thrust nor drag. The
hind limbs, which develop externally, may
add slightly to drag, but do not contribute
to thrust. Thus, with anuran larvae axial
locomotion is independent of appendicular
locomotion. In addition, the axial musculature of tadpoles is structurally much simpler than that of fishes. Thus modelling
muscle function should, in theory, be simpler in tadpoles.
A review of anuran kinematics suggests
that, despite their simple locomotor system, these organisms are surprisingly effective swimmers. Their kinematics are, in
fact, similar to subcarangiform fishes and
they can, for example, achieve maximum
velocities comparable to those recorded for
those fishes. However, tadpoles lack the
ability of many fishes to sustain high swimming speeds or execute intricate mid-water
maneuvers. I have suggested that the dif-
ferences in swimming behavior between
anuran larvae and teleost fishes reflect
structural specializations of tadpoles, which
are dictated by their need to undergo rapid
metamorphosis. I have focused on two such
features: the tadpole's floppy tail and its
hidden anterior appendages. These features may be linked in the following way:
All anuran larvae lack caudal vertebrae
and must depend on musculature for both
the generation of thrust and, to a large
extent, for skeletal support (stiffness regulation). The greater flexibility associated
with the absence of an osseous skeleton
gives tadpoles a shorter turning radius than
one would expect for typical teleost fishes
of the same size, whose fins and central axis
are stiffened by cartilage and bone. At the
same time, the absence of caudal vertebrae
in tadpoles allows for more rapid resorption of the caudal propulsor at metamorphosis than would be possible with bone
present. Without caudal vertebrae, tadpoles use muscle activity to adjust flexibility within regions of the tail and effect
turning. By depending solely on axial
mechanisms for turning, tadpoles do not
need lateral appendages for this action.
This "frees-up" those appendages to
develop directly into the adult limbs. By
having the anterior ones develop under an
opercular fold, the adult forelimbs can
appear {i.e., erupt) fully formed and functional at the instant of metamorphosis,
concurrent with the rapid resorption of the
tail. Thus, the unusual tail of tadpoles and
the development of their forelimbs within
an opercular chamber appear to be related
features that together allow tadpoles both
efficient larval locomotion and the ability
to transform rapidly at metamorphosis into
frogs.
The locomotor morphology of tadpoles
is both radically different from that of other
aquatic vertebrates and at the same time
diverse within the Anura. Larvae of different species of frogs differ in their locomotor kinematics. Furthermore, motor
activity along the tail of any single tadpole
may differ greatly as a function of velocity
and acceleration. Comparison of the kinematics and morphology of Xenopus vs.
LOCOMOTION IN AMPHIBIAN LARVAE
Rana—two extremes in larval behavior and
design—give some insight into how differences in skeletal structure (e.g., notochord)
and neuromuscular pattern (e.g., spinal
nerve arrangement) among species relate
to differences in the swimming behavior of
these animals.
As a final note, anurans are not the only
organisms whose larvae are called "tadpoles." The tunicate larvae, with their globose bodies and distinct tails, share both
the shape and name. Tunicates, of course,
lack vertebrae in their tails by definition.
However, it may be more than a coincidence that their larvae are built similarly
to tadpoles, for they too go through an
abrupt metamorphosis.
ACKNOWLEDGMENTS
This paper developed out of my long
term collaboration on the functional and
evolutionary morphology of amphibian
larvae with Karin v. S. Hoff. Most of the
ideas in this paper come directly from that
association.
Kiisa Nishikawa has collaborated with us
in studying the nervous system of tadpoles.
Nisar Huq and V. Ann King helped collect
and analyze kinematic data on salamander
larvae. Ann King provided expert technical help as well with many aspects of histology, illustration, and microphotography. This study has profited greatly from
discussions with David Chapman, Donald
Stehouwer, Marvalee Wake and Daniel
Weihs. I thank them all, plus David Cannatella, Robert Dudley, Robin Dushman,
Robert Full, Carl Gans, Harry Greene, Patrick Jackson, Michael Lannoo, Tomio Naitoh, Kiisa Nishikawa, Ellengene Peterson,
Stephen Wainwright and Paul Webb for
constructive comments on the manuscript.
The Department of Zoology and
Museum of Vertebrate Zoology, University of California, Berkeley housed and
intellectually fed me during the crucial
period when thoughts were transformed
to written words. I most gratefully thank
the Natural Science and Engineering
Research Council of Canada for their continued support of my studies on larval
amphibians.
81
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