657
INTRODUCTION
Sand lances (Family Ammodytidae) are a group of fishes that
employ anguilliform locomotion during pelagic swimming, and
exhibit a peculiar behavior of actively swimming into sandy
substrates as a refuge (Dick and Warner, 1982). This burrowing
behavior is associated with hibernation during the winter, daily
migrations into the sand after dark and predator avoidance
(Winslade, 1947a; Winslade, 1947b; Girsa and Danilov, 1976). The
burrowing behavior of sand lances presents a good opportunity to
investigate the mechanics of both locomotion within and transitions
between different environments.
Seawater behaves as a Newtonian fluid and will flow continuously
when a shear stress is applied, whereas a sand–water mix may act
as a non-Newtonian fluid, because of both sand–sand and
sand–water interactions. Settled wet sand is a hybrid material with
some solid and some fluid properties, and it will generally support
some shear stress. The precise mechanics of particle interaction
remains unclear, although similar ‘frictional fluid’ sand–air mixtures
have been studied (Maladen et al., 2009).
During terrestrial locomotion, snakes and other limbless
vertebrates use undulatory locomotion whereby they apply force to
discrete, non-moving points on the ground via a posteriorly
propagating wave (Gray, 1946). In the ideal case, where these points
are immobile, the animal’s propulsive undulations travel caudally
along the body, maintaining a velocity equal, though oppositely
oriented, to the animal’s forward progress (Jayne, 1986).
Consequently, all points along the axis of the body will follow the
same trajectory: the undulatory wave, which, while propagating
posteriorly along the animal’s body, will not move in a world-based
coordinate system (Jayne, 1986). We will refer to this mode of
locomotion as ‘non-slipping wave’ locomotion.
By contrast, animals using aquatic undulatory locomotion do
not have discrete push points available because they are exerting
force onto a fluid for propulsion. Because water continuously
deforms under shear stress, the water will flow as the body of an
animal pushes against it. Also, because flow results in undulatory
waves that move in a world-based coordinate system, all points
along the body’s axis will not follow the same trajectory (Grillner
and Kashin, 1976; Gillis, 1998). In this case, the undulatory waves
move posteriorly with respect to both the body and the world.
We will refer to this mode as ‘slipping wave’ locomotion. In a
study comparing the mechanics of undulatory locomotion on land
and in water, Gillis (Gillis, 1998) studied kinematic differences
in the eel, Anguilla rostrata (Lesueur 1817). Effectively, eels
traveling on land locomote using nearly non-slipping wave
locomotion (more like other terrestrial vertebrates), whereas
those same individuals engage in slipping wave locomotion in an
aquatic environment (Fig.1).
The Journal of Experimental Biology 214, 657-664
© 2011. Published by The Company of Biologists Ltd
doi:10.1242/jeb.047068
RESEARCH ARTICLE
Locomotory transition from water to sand and its effects on undulatory kinematics in
sand lances (Ammodytidae)
Nicholas J. Gidmark
1,
*, James A. Strother
2
, Jaquan M. Horton
3
, Adam P. Summers
3
and Elizabeth L. Brainerd
1
1
Department of Ecology and Evolutionary Biology, Brown University, Providence, RI 02912, USA,
2
Department of Ecology and
Evolutionary Biology, University of California, Irvine, Irvine, CA 92697, USA and
3
Friday Harbor Laboratories, University of
Washington, Friday Harbor, WA 98250, USA
*Author for correspondence (gidmark@brown.edu)
Accepted 21 October 2010
SUMMARY
Sand lances, fishes in the genus Ammodytes, exhibit a peculiar burrowing behavior in which they appear to swim rapidly into the
substrate. They use posteriorly propagated undulations of the body to move in both water, a Newtonian fluid, and in sand, a non-
Newtonian, granular substrate. In typical aquatic limbless locomotion, undulations of the body push against water, which flows
because it is incapable of supporting the static stresses exerted by the animal, thus the undulations move in world space
(slipping wave locomotion). In typical terrestrial limbless locomotion, these undulations push against substrate irregularities and
move relatively little in world space (non-slipping wave locomotion). We used standard and X-ray video to determine the roles of
slipping wave and non-slipping wave locomotion during burrowing in sand lances. We find that sand lances in water use slipping
wave locomotion, similar to most aquatic undulators, but switch to non-slipping waves once they burrow. We identify a
progression of three stages in the burrowing process: first, aquatic undulations similar to typical anguilliform locomotion (but
without head yaw) push the head into the sand; second, more pronounced undulations of the aquatic portion of the body push
most of the animal below ground; third, the remaining above-ground portion of the body ceases undulation and the subterranean
portion takes over, transitioning to non-slipping wave locomotion. We find no evidence that sand lances use their body motions
to fluidize the sand. Instead, as soon as enough of the body is underground, they undergo a kinematic shift and locomote like
terrestrial limbless vertebrates.
Key words: Ammodytes, burrowing, anguilliform locomotion, serpentine locomotion.
THEJOURNALOFEXPERIMENTALBIOLOGY