The Journal of Experimental Biology
3742
© 2014. Published by The Company of Biologists Ltd | The Journal of Experimental Biology (2014) 217, 3742-3747 doi:10.1242/jeb.108506
ABSTRACT
A controlled landing, where an animal does not crash or topple,
requires enough stability to allow muscles to effectively dissipate
mechanical energy. Toads (Rhinella marina) are exemplary models
for understanding the mechanics and motor control of landing given
their ability to land consistently during bouts of continuous hopping.
Previous studies in anurans have shown that ground reaction forces
(GRFs) during landing are significantly higher compared with takeoff
and can potentially impart large torques about the center of mass
(COM), destabilizing the body at impact. We predict that in order to
minimize such torques, toads will align their COM with the GRF
vector during the aerial phase in anticipation of impact. We combined
high-speed videography and force-plate ergometry to quantify
torques at the COM and relate the magnitude of torques to limb
posture at impact. We show that modulation of hindlimb posture can
shift the position of the COM by about 20% of snout–vent length.
Rapid hindlimb flexion during the aerial phase of a hop moved the
COM anteriorly and reduced torque by aligning the COM with the
GRF vector. We found that the addition of extrinsic loads did not
significantly alter landing behavior but did change the torques
experienced at impact. We conclude that anticipatory hindlimb flexion
during the aerial phase of a hop is a critical feature of a mechanically
stable landing that allows toads to quickly string together multiple,
continuous hops.
KEY WORDS: Landing, Ground reaction force, COM, Stability,
Hopping, Pitching moment
INTRODUCTION
Landing after a hop or jump is a common locomotor task among
terrestrial organisms. These locomotor events can pose a significant
biomechanical challenge given the large ground reaction forces
(GRFs) associated with such impacts (Nauwelaerts and Aerts, 2006;
Ericksen et al., 2013). Large GRFs can pose a potential danger to
the bones, ligaments or muscles of the limbs, which are tasked with
rapidly dissipating mechanical energy and decelerating the body
(Aerts et al., 2013). Strategies used to ensure a safe landing often
involve anticipatory motor control strategies (Santello, 2005) and
modulation of limb posture prior to impact (Wikstrom et al., 2008).
Anticipatory muscle recruitment, which is associated with landings
across a diverse array of taxa (Dyhre-Poulsen and Laursen, 1984;
Santello and McDonagh, 1998; Prochazka et al., 1977; Gillis et al.,
2010), is thought to increase joint stiffness and allow for more
effective energy dissipation by muscles (Horita et al., 2002; Santello,
2005). Furthermore, proper alignment of the limb at impact can
RESEARCH ARTICLE
Department of Ecology and Evolutionary Biology, University of California, Irvine,
Irvine, CA 92697, USA.
*Author for correspondence (eazizi@uci.edu)
Received 22 May 2014; Accepted 16 August 2014
minimize the stresses experienced by skeletal elements and
ligaments during landing (Wikstrom et al., 2008; Norcross et al.,
2013).
In addition to possible injury, large GRFs associated with impact
have the potential to destabilize the body during landing. These large
GRFs can produce significant torques if they act with even a modest
moment arm relative to the center of mass (COM). The excessive
torques experienced during landing can produce a pitching or rolling
moment about the COM, which can cause an organism to stumble
or crash. One strategy to improve stability during landing is to use
movements of the torso and the forelimbs to better align the COM
with the GRF vector (Bates et al., 2013). Such changes in posture
can stabilize the body by either reducing or quickly counteracting
torques experienced at the COM (Blackburn and Padua, 2008).
Thus, a safe and stable landing often involves an intricate interplay
of limb and body configuration.
Although most anurans are considered highly specialized jumpers
or hoppers, toads (Family: Bufonidae) are particularly effective at
landing. In most anurans, the movements associated with the takeoff
phase of a hop or jump are largely conserved (Zug, 1985). In
contrast, the mechanics of landing tend to vary significantly among
different anuran radiations. For example, species from basal
radiations tend to land rather inelegantly, performing what amounts
to a ‘belly flop’ during each landing (Essner et al., 2010). This
pattern has led to the hypothesis that a finely tuned landing behavior
may be a derived characteristic among certain radiations (Essner et
al., 2010). Landing is also rather inconsistent in semi-aquatic species
(Family: Ranidae), where the chest, torso or legs frequently contact
the substrate during landing (Nauwelaerts and Aerts, 2006; Essner
et al., 2010). However, landing behavior in toads is characterized by
a controlled deceleration accomplished solely with the forelimbs
(Gillis et al., 2010; Akella and Gillis, 2011). During landings, toads
appear balanced and stable, providing sufficient time for the muscle
of the forelimbs to dissipate energy and slow the body before gently
bringing the hindlimbs toward the ground (Azizi and Abbott, 2013;
Azizi, 2014).
Similar to landings in other organisms, stable and well-
coordinated landings in toads are thought be associated with
anticipatory motor strategies prior to impact. The intensity of
activation in the muscles of the forelimbs has been shown to be
tuned to the perceived magnitude of the impending impact (Gillis et
al., 2010). This tuning of forelimb activity can help to stiffen joints
in anticipation of large impacts (Gillis et al., 2010) and also shift
where landing muscles operate on the force–length curve (Azizi and
Abbott, 2013). Anticipatory strategies may not be limited to the
forelimbs but could also include changes in body angle or postural
changes in the hindlimbs.
In this study, we used cane toads, Rhinella marina (Linnaeus
1758), as a model system to examine how hindlimb posture during
landing affects the stability of the whole body. Previous studies have
shown that the hindlimbs can make up more than 30% of body mass
Reduce torques and stick the landing: limb posture during
landing in toads
Emanuel Azizi*, Neil P. Larson, Emily M. Abbott and Nicole Danos