AMER. ZOOL.

, 36:723-735 (1996)

Springs in Swimming Animals'

D. ANN PABST

Biological Sciences and Center for Marine Science Research,

University of North Carolina at Wilmington,
Wilmington, North Carolina 28403
SYNOPSIS. Animals can lower the metabolic cost of swimming by using
appropriately tuned, elastic springs. Jet-powered invertebrates use springs
that lie in functional parallel to their swimming muscles to power half
the locomotor cycle. The parallel geometry constrains the spring to be
non-linearly elastic; muscle power is diverted to load the spring only
when swimming muscles are not capable of producing maximal hydrodynamic thrust. The springs of jellyfish and scallops are forced at or near
their resonant frequency, producing large energy savings. Measuring the
contribution of elastic energy storage to jet-powered locomotion has been
facilitated by the relatively simple geometries of invertebrate locomotor
systems. In contrast, complex musculoskeletal systems and kinematics
have complicated the study of springs in swimming vertebrates. Skins,
tendons and axial skeletons of some vertebrate swimmers have appropriate mechanical properties to act as springs. To date, though, there exist
just a handful of studies that have investigated the mechanical behaviors
of these locomotor structures in swimming vertebrates, and these data
have yet to be integrated with measures of swimming power. Integrating
mechanical, kinematic, hydrodynamic and metabolic data are required to
understand more fully the role of elastic springs in vertebrate swimming
energetics.

(Daniel, 1991; Triantafyllou and TriantafylThis paper investigates mechanisms that lou, 1995).
Animals can reduce resistive forces by
large animals use to decrease the energetic
optimizing
body shapefor example,
costs of swimming. To swim, animals must
in
fishes, squids and cetaceans
streamlining
produce thrust forces greater than or equal
(e.g.,
Slijper,
1936;
Webb, 1982, 1984;
to the resistive forces they experience
(Weihs and Webb, 1983; Vogel, 1994). Weihs and Webb, 1983; Fish and Hui,
Generation of thrust forces by locomotor 1991; Vogel, 1994). Behavioral adaptations,
muscles requires metabolic energy. The such as burst and glide swimming and poramount of metabolic energy used to swim poising, also theoretically decrease the recan be reduced by either (1) reducing the sistive forces experienced by swimmers
resistive forces the animal experiences and/ (Weihs, 1973; Au and Weihs, 1980; Videler
or (2) increasing thrust efficiency (Daniel and Weihs, 1982; Blake, 1983). These
and Webb, 1987; Vogel, 1994). Thrust ef- swimming styles alternate periods of relaficiency will be defined here as the ratio of tively high-drag body undulations with pethrust power (mean thrust times speed) rel- riods of relatively low-drag straight body
ative to the rate of metabolic energy used coasting and, thus, likely lower the overall
cost of transport relative to steady, undulatory swimming.
1
From the Symposium Aquatic Locomotion: New
Animals may increase their thrust effiApproaches to Invertebrate and Vertebrate Biome- ciency by capturing kinetic energy from the
chanics presented at the Annual Meeting of the Society
for Integrative and Comparative Biology, 2730 De- fluid flowing around their bodies. Kinetic
energy contained in vortices shed from
cember 1995, at Washington, D.C.
INTRODUCTION

723

724

D. ANN PABST

parts of their own bodies, or from those of

their schoolmates, may be recaptured to increase thrust power (Weihs, 1973; Gopalkrishnan et al., 1994; Triantafyllou and
Triantafyllou, 1995). Cetaceans increase
their thrust efficiency by "surfing" waves
(e.g., Bose and Lien, 1990; Williams et al,
1992; Fish, 1993a) and salmonids use advantageous eddy flows to power upstream
swimming (Triantafyllou and Triantafyllou,
1995).
Animals can also capture, temporarily
store, and release kinetic energy in internal
elastic structures that are strained during locomotion (Daniel, 1991 and 1995). These
elastic springs can reduce the inertial work
required of muscles to decelerate and re-accelerate the propulsive "appendage"
whether it be the whole body, caudal fin or
pectoral fin. The role of stored elastic strain
energy, although well documented in terrestrial animals {e.g., Alexander and Bennet-Clark, 1977; Alexander and Vernon,
1975; Cavagna et al., 1977; Biewener and
Baudinette, 1995) and in swimming invertebrates (see below), remains controversial
in swimming vertebrates (e.g., Blickhan
and Cheng, 1994). The goals of this paper
are to (1) briefly review the types of evidence that have been used to characterize
the role of springs in locomotor energetics,
(2) compare parallel and in-series springs,
(3) describe how springs work during invertebrate jet propulsion and (4) discuss existing evidence for the role of springs in
swimming vertebrates. This discussion will
reveal that, to date, no study has integrated
data on spring mechanics, kinematics, force
output, and metabolic energy use in any
swimming vertebrate. The role of springs in
vertebrate swimming is apt to remain controversial until such data exist.
EVIDENCE OF THE ROLE OF SPRINGS IN
LOCOMOTOR ENERGETICS

Three broad categories of studies have

contributed to our understanding of elastic
strain energy storage. Most of the following
examples are from studies on terrestrial animals. Metabolic data alone suggest that
springs are functioning in some animals.
For example, red kangaroos (Dawson and
Taylor, 1973) and tammar wallabies (Bau-

dinette et al, 1992) can almost triple their

hopping speeds without increasing their
metabolic rate, suggesting that some passive spring mechanism is contributing to locomotion.
The "Metabolic Approach" compares
calculated mechanical power required to
produce locomotor forces and movements
(Wmcch) to measured metabolic power used
(Wmct) (e.g., Cavagna et al, 1977). The efficiency of locomotion can be defined as the
ratio of Wmect/Wmet. If Wmech/Wmet is greater
than the maximum efficiency of locomotor
muscle, it can be logically deduced that locomotion is being powered in part by elastic springs (Wipring) (Alexander, 1988; Cavagna et al, 1977). (See also Dickinson and
Lighton, 1995, for a similar analysis of
springs in flying Drosophila.) The metabolic approach allows estimates of energy
savings due to springs, but does not identify
the spring. The "Mechanical Approach"
identifies the spring and, via material testing, defines its mechanical properties. Kinematic or force plate data are integrated
with spring mechanical behavior to estimate
Wspnng and compare it to either Wmech or
Wmel (e.g., Alexander and Vernon 1975; Ker
et al, 1987). The "Integrated Approach"
brings together data from both these approaches and often couples those data with
more direct measures of spring deformation
(e.g., Biewener and Baudinette, 1995; Daniel, 1995). Mechanical data characterizes
the spring. The history of spring strain
throughout a locomotor cycle is either estimated from kinematic records or measured directly with force or strain gauges.
The mechanical output of the animal, as
well as its metabolic energy usage are measured. Often, electromyographic (EMG) records define the timing and activity of the
locomotor muscles. The integrated approach offers a more detailed, mechanistic
view of how springs function during locomotion.
PARALLEL VS. IN-SERIES SPRINGS

Springs can be arranged in two different

geometries relative to locomotor muscles
(Bennett et al, 1987; Alexander, 1988)
(Fig. 1). Parallel springs undergo the same
displacement as the locomotor muscle, and

SPRINGS IN SWIMMING ANIMALS

725

In contrast, invertebrate swimmers use

exclusively parallel springs to store elastic
strain energy {e.g., Gosline and Shadwick,
1983; Johnsen and Kier, 1993). Both in-series (Bennett et al, 1987; Blickhan and
Cheng, 1994) and parallel (Wainwright et
al., 1978; Alexander, 1987; Pabst, 1996)
springs have been implicated in vertebrate
swimmers.
Swimming animals do not "bounce off"
of a hard substratehow do their springs
function? Both resonant and non-resonant
locomotor systems have been described in
swimming animals. For any spring-mass
system, there is a natural frequency at
which the system will oscillate (reviewed in
Alexander, 1988 and Farley et al., 1993).
At this frequency, the elastic restoring force
of the spring and the inertial force due to
acceleration of the mass, are equal in amplitude, but opposite in directionthus,
these forces cancel. The energy required to
A
B
drive a spring-mass system with an external
FIG. 1. Spring geometries. Passive elastic springs can force is dependent upon the frequency at
lie either (A) parallel to or (B) in-series with locomotor which the force is applied. Muscles driving
muscles. Muscles and parallel springs undergo the a locomotor system at frequencies well besame displacement and their forces are additive. Mus- low its natural frequency will use metabolic
cles and in-series springs experience the same force
and their displacements are additive. The central plate energy to deform spring elements. Muscles
represents propulsive appendage. (Adapted from Ben- driving a locomotor system at frequencies
nett et al., 1987).
well above its natural frequency will use
metabolic energy to accelerate the mass of
spring and muscle forces are additive. In- the system. But when a system is continuseries springs experience the same force as ously driven at or near its natural frequency,
the muscle, and spring and muscle displace- the exchange of elastic spring energy and
inertial energy eliminates the need for musments are additive.
cles
to deform spring elements or accelerate
Terrestrial animals use almost exclusivethe mass of the system. Metabolic energy
ly in-series springs to help power locomo- is required only to start the system moving,
tion. Most of the elastic strain energy is and to overcome any damping in the sysstored in the long, relatively slender ten- temeither from viscous properties of the
dons of the distal limb {e.g., Alexander and spring or from hydrodynamic work of
Vernon, 1975; Alexander, 1988; Biewener thrust production.
and Baudinette, 1995). Tendons and ligaments in the feet also function as in-series
In animals with non-resonant systems,
springs (Bennett et al., 1989; Ker et al., the energy stored in their springs comes
1987). These springs strain and temporarily from their own muscle energy. In these sysstore external energy (gravitational poten- tems, muscle energy is diverted to load the
tial and external kinetic) that is removed spring only when the muscles are not cafrom the animal's body as it contacts the pable of producing maximal hydrodynamic
ground. Long aponeurotic tendons of epax- thrust. Energy stored temporarily in springs
ial locomotor muscles may also function as may help power the next locomotor phase,
in-series springs that temporarily store in- allowing fuller utilization of muscles. External kinetic energy during the aerial phase amples of both resonant and non-resonant
systems are described below.
of galloping (Alexander et al., 1985).

726

D. ANN PABST

Tunic

Tunic
circular m.
FIG. 2. Schematic representation of squid (Loligo opalescens) mantle. Circular muscles wrap the circumference
of the mantle and power the jet phase. Radial muscles traverse the thickness of the mantle. Tunics formed by
helically wrapped collagen fibers limit mantle length changes. Two sets of obliquely oriented collagen fibers (1
and 2) traverse the mantle wall and are put into tension when the circular muscles contract. The third set of
collagen fibers (3) lies parallel to the circular muscles and does not function as springs during the jet phase.
(Adapted from Gosline and DeMont, 1985.)

SPRINGS IN INVERTEBRATE JET PROPULSION

Squids, hydromedusan jellyfish and scallops use jet propulsion to swim (Alexander,
1966; Gosline and Shadwick, 1983; Daniel,
1985; DeMont and Gosline, 1988a, b, c;
DeMont, 1990, Marsh et al, 1992). Thrust
is produced when water is forcefully expelled from an internal cavity through a
small diameter aperture (Daniel, 1985). Hydromedusans and scallops possess only one
set of locomotor muscles that power the
forceful jet phase of swimming; the recovery phase is powered exclusively by passive, elastic springs (Alexander, 1966; Daniel, 1985; DeMont, 1990). Although squids
possess two sets of antagonistic muscles
that could alternately power the jet and recovery phases, most of the recovery phase
is powered by passive springs (Gosline and
Shadwick, 1983).
I will focus on two "Integrated" studies
of invertebrate swimmersthose on squid
(non-resonant system) by Gosline and his
colleagues (Gosline and Shadwick, 1983;
Gosline et al., 1983; Gosline and DeMont,
1985 and based upon the morphological
studies of Ward and Wainwright, 1972) and
those on hydromedusan jellyfish (resonant
system) by DeMont and Gosline (1988a, b,

c). Both animals possess geometrically simple locomotor systems.

Squid jetting is powered by muscles and
collagenous springs in the mantle wall (Fig.
2). Two sets of muscles form the mantle:
(1) circular muscles that power the jetphase of locomotion, and (2) radial muscles
that traverse the thickness of the mantle
wall and can power the refilling (recovery)
phase. The inner and outer surfaces of the
mantle are formed by helically wrapped
collagenous tunics that resist changes in
mantle length. Two sets of obliquely oriented collagen fibers traverse the thickness
of the mantle wall in both longitudinal and
transverse body planes and act as springs.
As a constant volume system, the squid
mantle functions as a muscular-hydrostat
(reviewed by Kier and Smith, 1985; Smith
and Kier, 1989). Thus, when the circular
muscles contract (shorten) they must also
increase in diameter, which causes the mantle wall to thicken. The obliquely oriented
collagen fibers that traverse the thickness of
the mantle will be strained and temporarily
store energy.
Can that strain energy be used to help
power the recovery phase and reduce the
work required of the radial muscles? Be-

SPRINGS IN SWIMMING ANIMALS

cause the energy that is temporarily stored

in the collagen fibers comes directly from
muscle contractions, the spring must only
be loaded at times in the locomotor cycle
when the circular muscles "cannot apply
their full mechanical output to generating
useful hydrodynamic thrust" (Gosline and
Shadwick, 1983). Thus, analyzing the efficacy of the mantle spring requires simultaneous measures of (1) thrust or hydrodynamic work (H), (2) muscle work capacity
(M), (3) spring energy stored and (4) muscle activity patterns, integrated over the duration of the jet cycle.
Because the squid body (Loligo opalescens) can be modeled as a circular cylinder
with a constant volume cylinder wall, simultaneous measures of internal mantle
cavity pressure and external mantle diameter could be used to calculate H and M
(Gosline and Shadwick, 1983). H is simply
internal mantle cavity pressure multiplied
by the volume of fluid expelled. M is simply muscle force (muscle stress X muscle
cross-sectional area) multiplied by the
change in length of muscle fibers. Muscle
efficiency was defined as E = H/M. Volume, cross-sectional area of mantle muscle
and muscle fiber length changes could be
calculated from measured changes in the
external diameter of the mantle.
At the initiation of the jet cycle, the pressure inside the mantle cavity is high, and
the radius decreases quickly, indicating that
the circular muscles are producing large hydrodynamic forces at high efficiencies (Fig.
3). During the second half of the jet cycle
pressure drops, despite continued decreases
in mantle diameter, and E drops precipitously.
The muscle energy that is not producing
useful hydrodynamic work could be captured {i.e., not wasted) during the second
half of the jet phase by loading the mantle
springif the muscles continued to contract
at maximal force and if the spring had precisely tuned mechanical properties. The
mechanical properties required of the spring
could be predicted based upon the efficiency data (Fig. 3). Stress-strain data demonstrated that the non-linearly elastic mantle
spring had appropriate stiffness and resilience to power the recovery phase. EMG

727

studies (Gosline et ai, 1983) demonstrated

that most of the power required to refill the
mantle cavity comes from elastic energy
storage, and only a small amount from radial muscles.
Thus, the mantle spring plays an important mechanical role in the non-resonant,
squid locomotor system. It stores elastic
strain energy at a time in the jet cycle when,
because of the geometry of the locomotor
apparatus, the circular muscles cannot do
useful hydrodynamic work. That stored energy is available to initiate the subsequent
recovery phase, and may decrease the
amount of radial muscle required for jetting. Thus, the circular muscles act directly
during the jetting phase and indirectlyvia
the mantle springduring the recovery
phase. The mantle spring appears to allow
the circular muscle to do useful work
throughout the entire jet, potentially increasing power output per unit muscle mass
and improving acceleration of the jet.
Because the parallel springs and muscles
undergo similar deformations during locomotion (see Fig. 1), the circular muscle
must do work, at all times of the jet phase,
to load the spring. Thus, the parallel arrangement of the muscles and spring constrains the spring to be non-linear. The initial low stiffness of the mantle spring (see
Fig. 3c) suggests that little muscular force
is diverted to load the spring during the initial portion of the jet phase, when the swimming muscles are performing maximal hydrodynamic work. When the potential for
doing useful hydrodynamic work decreases,
the increased stiffness of the mantle spring
permits elastic strain energy storage. Thus,
we can predict that any spring in functional
parallel to swimming muscles should have
a non-linear stress-strain curve.
DeMont and Gosline (1988a, b, c) investigated the mechanics of swimming in the
hydromedusan jellyfish (Polyorchis penicillatus), an animal that also uses parallel
springs to power swimming (see also Daniel, 1983, 1985 and 1995). Using techniques similar to those of Gosline and
Shadwick (1983), these authors simultaneously measured internal subumbrellar
cavity pressure and internal bell diameter.
From these measurements, the forces re-

728

D. A N N PABST

22.5
.

15.0

\ Pressure (kPa)

7.5
0

1.3- ". radius (cm)

1.1 - \
0.9
0.2

0.6

1.0

time (s)

100

100

80

80
>>
c 60

60

ftici

0)

o 40
LU

LU

20
0

0 0.2

0.4

0.6 0.8

40
20

Energy "available"

-W
r

0
0.9

F 1.0.

time (s)

1.1

. A
1.3

1.2

radius (cm)

w 0.1

-0.1 -0.2 -0.3 -0.4

strain

FIG. 3. How the squid's (Loligo opalescens) mantle spring functions. A. Pressure within the mantle cavity
increases and mantle radius decreases rapidly at the beginning of the jet phase. B. The squid body can be
modeled as a circular cylinder with a constant volume wall; simultaneous measures of internal mantle cavity
pressure and external mantle diameter yield calculations of hydrodynamic work (H) and muscle work (M).
Muscle efficiency is defined as E = H/M. E drops precipitously during the second half of the jet phase. As the
radius decreases, the amount of energy "available" increases. A tuned spring could capture the available energy.
C. The stress-strain curve for squid mantle tested in compression (solid line). The separate points indicate
predicted stress-strain values derived from the relationship between radius and energy available. The mechanical
properties of the mantle spring suggest that it can capture and release muscle energy that is not being used to
produce hydrodynamic thrust. (Adapted from Gosline and Shadwick, 1983.)

SPRINGS IN SWIMMING ANIMALS

quired of the locomotor muscles to (1) do

useful hydrodynamic work, (2) overcome
inertia of the bell and (3) and deform the
bell could be calculated. Thus, this study
attempts to quantify all work done by muscles. Hydrodynamic forces were calculated
as in Gosline and Shadwick (1983). Inertial
forces were calculated by multiplying the
acceleration of the bell (using the second
derivative of diameter change) by the mass
of the of the animal plus the added mass of
water both in inside and outside the subumbrellar cavity. By modeling the bell as a
circular cylinder with a mesogleal wall of
constant volume, pressurevolume relationships were converted to stress-strain values.
Thus, the stiffness of the bell and the energy required to deform it could be calculated.
During contraction of the circular locomotor muscles, radial mesogleal fibers in
the bell are strained and store energy. The
bell spring has a non-linear stress-strain
curve, as would be predicted for any parallel spring. Because of the geometry of the
swimming apparatus, the ability of the circular muscles to produce hydrodynamic
work falls during the last half of the jet
phase. The energy required to produce hydrodynamic work is about two times larger
than that required to overcome inertia or to
deform the bell during locomotion. The energy stored in the bell spring and released
was calculated to be similar to that required
to power the refilling stage. Thus, the bell
spring is capable of storing sufficient energy to power the refilling phase.
DeMont and Gosline (1988c) modeled
the jellyfish as a moderately damped, forced
oscillator and discovered that these animals
swam at or near their resonant frequency
(approximately 1 Hz). Thus, jellyfish can
achieve relatively high amplitude deformations of the bell without expending energy
to deform the spring or move the system's
mass. The total metabolic cost of swimming
at resonance is between 2437% lower than
that of swimming off resonance (DeMont
and Gosline, 1988c). Marsh et al. (1992)
and DeMont (1990) have used similar experimental and computational designs to
suggest that scallops also swim using jet cycles at or near their resonant frequency.

729

SPRINGS IN SWIMMING VERTEBRATES

The contributions of elastic springs to the

swimming energetics of squids, hydromedusan jellyfish and scallops could be calculated because of the relatively simple geometries of their locomotor systems. We
know relatively less about the role of elastic
energy storage in swimming vertebrates. It
is quite understandable given the (1) complex nature of vertebrate musculoskeletal
systems and swimming kinematics and (2)
difficulties in accurately modeling complex
fluid flows and, thus, calculating hydrodynamic forces. While there have been consistent advances in our understanding of
swimming physiology {e.g., Brill, 1996;
Williams et al., 1993; Dewar and Graham,
1994a), force transmission systems (van
Leeuwen et al., 1990; Altringham et al.,
1993; Pabst, 1993; Rome et al, 1993;
Westneat et al., 1993), and hydrodynamic
theory {e.g., Yates, 1983; Cheng and Blickhan, 1994), there are, to date, no integrative
studies that assay the role of elastic energy
storage in swimming vertebrates. There exist, though, multiple lines of evidence that
suggest springs may be used to power locomotion in some fishes and cetaceans.
Skins and skeletons as springs
Mechanical testing of isolated locomotor
structures have revealed that some swimming vertebrates possess skins and axial
skeletons that behave like springs. The skin
of lemon sharks {Negaprion brevirostris),
for example, reinforced with multiple layers
of helically wound collagen fibers, is a resilient, non-linearly elastic spring in functional parallel to the axial swimming muscles (Fig. 4) (Wainwright et al., 1978). The
stiffness of the skin and, thus, the strain energy it can store, increases with increased
swimming speed. Wainwright et al. (1978)
hypothesized that energy stored in the skin
is released at the extreme point of lateral
body flexure, when muscles on the convex
side of the body are presumably stretched
to a disadvantageous length for generating
force effectively. The elastic recoil would
accelerate body unbending, and increase
hydrodynamic power.
Although Wainwright et al. (1978) did

730

D. ANN PABST

and inertial work, coupled with data on skin

strain, are required to test this hypothesis.
The skin of the American eel {Anguilla
rostratd) behaves similarly to shark skin
when loaded biaxially under pseudostatic
conditions (Hebrank, 1980), but the skins
E 4.0
of Norfolk spot (Leiostomus xanthurus) and
skipjack tuna {Katsuwanus pelamis) do not
^ 3.0
(Hebrank and Hebrank, 1986). Although
Hebrank and Hebrank (1986) do not mea 2.0
sure skin resilience, spot and tuna skin do
a1
0
not deform like crossed-fiber systems and
do
not appear to behave like springs. It
a
would
be profitable to repeat these tensile

0
-20
-10
0
+10 +20 +30 +40 +50
tests on fish skins using dynamic biaxial
testing regimes that better mimic skin loadLongitudinal elongation (%)
ing in vivo, since strain rate can alter the
FIG. 4. Longitudinal stress-strain behavior of lemon
shark (Negaprion brevirostris) skin under biaxial ten- mechanical properties of biological materision. Upper panel illustrates the orientation of some of als (Wainwright et al., 1976).
the collagen fibers that reinforce the skin. The lower
The skins of most other cylindrically
curve is for skin held at a constant 0.3 MN/m2 circumferential stress experienced during slow cruising. The shaped, swimming vertebrates are also reupper curve is for skin held at a constant 2.8 MN/m2 inforced with helically wound collagen ficircumferential stress experienced during fast swim- bers that anchor onto underlying axial skelming. Notice the skin is non-linearly elastic and its etal elements (reviewed in Pabst, 1996). Alstiffness increases with increased swimming speed.
The energy stored in the skin spring may be released exander (1987) created a mathematical
at the extreme point of lateral body flexure, when mus- model, based upon helical geometry, that
cles on the convex side of the body are presumably predicts strains experienced by collagenous
stretched to a disadvantageous length for generating skin fibers when the cylinder undergoes
force effectively. The elastic recoil would accelerate bending. Alexander's model predicts that
body unbending, and increase hydrodynamic power.
60 is the critical fiber angle at which bend(Adapted from Wainwright et al., 1978.)
ing neither causes stretching nor shortening
of the skin fibers. The model predicts that
not analyze hydrodynamic forces experi- at fiber angles greater than 60, bending
enced by the swimming sharks, Gosline and causes a net increase in fiber strain, making
Shadwick (1983) hypothesized that if the the straight position stable. Collagen fibers
collagenous skin spring was loaded at a in the caudal peduncles of dolphins (Pabst,
time in the locomotor cycle when the swim- 1996), and in the tails of Norfolk spot and
ming muscles could not generate useful hy- skipjack tunas (Hebrank and Hebrank,
drodynamic thrust, it could function simi- 1986) describe helical angles greater than
larly to the mantle spring. In subcarangi- 60, and may act to store and release strain
form swimmers, calculations based upon energy when these vertebrate cylinders
slender body theory (Lighthill, 1975) dem- bend in swimming.
The axial skeleton undergoes bending in
onstrate that hydrodynamic power peaks at
mid-stroke, when the body is moving from parallel with locomotor muscles and could
a straight position to a bent position {e.g., store and release useful strain energy. PseuHess and Videler, 1984; Wardle et al, dostatic bending tests on segments of mar1995). Thus, the collagen fibers in shark lin (Makaira nigricans) backbones demonskin appear to be strained at a time in the strate that vertebral structures are non-linstroke cycle when the muscles are not pro- early elastic and between 60-80% resilient
ducing peak thrust power, suggesting that (Hebrank, 1982; Hebrank et al., 1990). Dyshark skin is an elastic spring working in a namic tests on individual intervertebral
non-resonant system. Kinematic data that joints of marlin demonstrate that the joints
could be used to calculate hydrodynamic are highly resilient (>90%) and can func-

. . - " " * ' ' ' ' ' ' "

SPRINGS IN SWIMMING ANIMALS

tion to store and release elastic energy when

joints move from a bent to an unbent position (Long, 1992). The notochord of sturgeon also appears mechanically capable of
storing and releasing elastic energy (Long,
1995), although this function has not been
specifically tested. The inter vertebral joints
of common dolphins {Delphinus delphis)
appear only to function as moderately resilient springs at high bending amplitudes
(Long et al., 1997). Pseudostatic bending
tests on vertebral columns of Norfolk spot
and skipjack tuna (Hebrank, 1982) suggest
that they do not function to store elastic
strain energy, although dynamic bending
tests on these backbones would further test
this result.
Dynamic mechanical data support the hypothesis that the marlin backbone functions
as an elastic spring, but the role of that elastic energy in whole animal swimming energetics remains unknown. Long (1992) has
calculated vertebral spring power for marlin, but there unfortunately exist no comparable data on muscular or hydrodynamic
power. Acquiring kinematic data, under
controlled conditions, that could be used to
estimate hydrodynamic work of large
swimming marlin is a daunting task, but
one necessary to fully understand the role
of elastic energy in these fish.
Dewar and Graham (1994a, b) have measured metabolic costs and kinematic parameters of swimming tunas. These kinematic
data could be used to calculate thrust power
using appropriate hydromechanical models
(for example, see Fish, 1993b). Dynamic
stress-strain tests on skin and dynamic
bending tests on intervertebral joints of
similarly sized tunas could be integrated
with metabolic and hydrodynamic power to
investigate the contributions of elastic energy storage to swimming energetics in
these high performance fishes. Tunas, unlike most fishes, also possess slender tendons that transmit muscle forces to the caudal peduncle and tail (Fierstine and Walters,
1968). These tendons may function as inseries springs and warrant further investigation.
Passive elastic structures play critical
roles in force transmission (Wainwright,
1983) and in establishing whole body stiff-

731

ness (see below). To date, though, there exist just a handful of studies that have investigated the mechanical behaviors of
these locomotor structures in swimming
vertebrates, and these data have yet to be
integrated with measures of swimming
power.
Whole body stiffness modulates undulatory
swimming
Fish swim by passing waves of bending
down their bodies; the shape and speed of
those waves, in turn, control thrust power
(Lighthill, 1975; McHenry et al., 1995).
Few studies have specifically investigated
the role of passive elastic structures in the
mechanics of wave propagation through the
fish body. Long (1996) discusses how fish
actively control body wave propagation.
Fish can be modeled as forced oscillatory
systems, i.e., as resonant systems {e.g.,
Blight, 1976, 1977; Long et al, 1994; McHenry et al., 1995). Thus, whole body stiffness will control the speed of wave propagation, and, in turn, the thrust power that
the fish can achieve. Whole body stiffness
depends, in part, upon the integrity of passive elastic structures. Wainwright et al.
(1978) demonstrated that the torsional stiffness of the lemon shark body is reduced by
half when the skin is cut. Long et al. (1994)
compared the angular bending stiffness of
whole dead pumpkinseed sunfish (Lepomis
gibbosus), "severed" fish (with skin intact,
but caudal horizontal septa, myotomes and
spinal nerves cut), and "ablated" fish (caudal musculature and skin removed). Each
disruption of locomotor structures was associated with a significant and large (50%
or greater) decrease in body angular stiffness. By electrically stimulating the dead
fish to swim, Long et al. (1994) discovered
that the speed and shape of the undulatory
wave was modulated, in part, by the passive
control of axial stiffness.
McHenry et al. (1995) investigated the
effect of body stiffness on undulatory
waveforms using anatomically accurate
models of pumpkinseed sunfish made of
homogeneous, isotropic vinyl. The models
were actuated via a bending couple applied
at the head. The "virtual" sunfish swam by
generating traveling waves of bending, sim-

732

D. ANN PABST

ilar to live fishes, supporting the hypothesis

that stiffness alone plays a critical role in
modulating the propulsive body wave
(Blight, 1976). Comparing swimming performances of vinyl vs. live fish demonstrated that live pumpkinseed must actively increase their body stiffness to twice that of
their passive body stiffness to achieve their
swimming speeds.
Thus, passive connective tissue structures
appear to play a significant role in modulating the mechanics of swimming by effecting whole body stiffness in a range of
fish species. Active control of body stiffness, though, is required to achieve performance levels observed in live swimming
fish. Muscles that act to increase body stiffness may do so by having tonus and by
loading elastic connective tissues during
swimming.
Do dolphins use springs to swiml
Dolphins swim by oscillating their caudal
tailstock and propulsive fluke blades (reviewed in Fish and Hui, 1991; Pabst, 1990,
1993). If dolphins possessed appropriately
tuned springs, elastic strain energy could be
used to replace some or all of the muscular
work required to decelerate and re-accelerate the flukes. Metabolic studies of swimming and exercising bottlenose dolphins
(Tursiops truncatus) suggest that elastic energy recovery may play a role in reducing
the metabolic cost of locomotion. Williams
et al. (1993) demonstrated that dolphins
swimming at 2 m/s incurred no more energetic cost than when resting. Dolphins
could also double their force output (above
some minimum value, as measured against
a stationary load cell) with no increase in
the rate of oxygen consumption. These data
suggest that dolphins may be using tuned
springs in a resonant system to decrease
their metabolic cost with increased speed
and force output.
The existence of elastic springs in swimming dolphins, though, has been a controversial topic (Bennett et al., 1987; Blickhan
and Cheng, 1994; Fish and Hui, 1991).
Bennett et al. (1987) investigated dolphin
springs using kinematic data from Lang and
Daybell (1963) and mechanical data from
isolated tendons and intervertebral joints.

These authors, using a simple hydromechanical model, calculated that dolphin tendons were too compliant to act as springs,
and, surprisingly, that they increased the
metabolic cost of swimming. Blickhan and
Cheng (1994) reevaluated the data presented in Bennett et al. (1987), calculating the
hydrodynamic forces experienced by the
flukes using three-dimensional unsteady
wing theory. The major difference between
these two studies was the calculation of the
hydrodynamic forces acting on the flukes.
Blickhan and Cheng (1994) calculated that
the mechanical properties of the in-series
tendons and intervertebral joints were near
optimal and could decrease the metabolic
cost of swimming in dolphins by as much
as 55%.
These two studies highlight the difficulties of assessing the role of elastic strain
energy in vertebrate swimming energetics.
The hydrodynamic forces experienced by
the dolphin's fluke blades were calculated
{i.e., not measured), in this case, by two different hydromechanical models, each with
its own set of simplifying assumptions (see
discussion in Cheng and Blickhan, 1994).
Available kinematic data were limited and
derived from one 0.8 second swimming record of a white-sided dolphin {Lagenorhynchus obliquidens), which may or may not
be representative of steady swimming in
most dolphins. (See Fish, 19936 for more
extensive kinematic analysis of dolphin
swimming.) Strains undergone by internal
connective tissues were estimated from
these kinematic data, not measured in vivo.
Finally, power required to swim was calculated from hydromechanical models, not
measured directly {i.e., rate of oxygen consumption).
Continued studies on dolphin swimming
energetics, though, should provide new insights into the role of elastic energy storage.
Dolphins, trained to swim against a load
cell while breathing into a metabolic hood,
can provide direct and simultaneous records
of hydrodynamic power and metabolic energy consumption {e.g., Williams et al.,
1993). Kinematic analyses of dolphins can
provide data from which phase and magnitude of spring deformation can be estimated {e.g., Wainwright et al., 1987). In-

SPRINGS IN SWIMMING ANIMALS

tegrating these data with spring mechanical

behavior can offer insights into the contribution of elastic strain energy to total locomotor energetics.
SUMMARY

The role of elastic energy storage is well

documented in invertebrates that swim via
jet-propulsion. The simple geometry of the
locomotor systems of these animals, and the
relative ease of experimental manipulation,
have led to precise understandings of spring
mechanics and energetics. Complex musculoskeletal systems, kinematics and hydrodynamic force patterns make it more difficult to gather the integrated data sets required to assess spring function in swimming vertebrates. Nonetheless, there is
evidence that skins, tendons and skeletons
of axial locomotors can function as springs,
and that passive body stiffness contributes
to modulating the propulsive body wave in
undulatory swimmers. Integrated studies,
coupling mechanical data, with kinematic,
metabolic and strain history data will
broaden our understanding of the role of
elastic energy storage in vertebrate swimming.
ACKNOWLEDGMENTS

Thanks to John Gosline, Margo Lillie,

Steve Katz, Bill McLellan and Steve Wainwright for energetic discussions on springs,
and to two anonymous reviewers whose insightful suggestions improved this paper.
This work was supported in part by a grant
from the Office of Naval Research
(N000149310751). This is CMSR contribution #148.
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