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First published online March 12, 2009
Journal of Experimental Biology 212, 945-953 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.026161
Bats go head-under-heels: the biomechanics of landing on a ceiling
1 Department of Ecology and Evolutionary Biology, Brown University, Providence,
RI 02912, USA
2 Division of Engineering, Brown University, Providence, RI 02912, USA
3 Institute of Biology, University of Southern Denmark, Campusvej 55, 5230
Odense M, Denmark
4 Center for Ecology and Conservation Biology, Boston University, 5 Cummington
Street, Boston, MA 02215, USA
* Author for correspondence (e-mail: dkr8{at}brown.edu)
Accepted 17 January 2009
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Summary |
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Key words: bats, manoeuvrability, roosting ecology
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Klem,
1990). Thus, any flying animal must be able to decelerate in a
controlled manner from its preferred flight speed before landing. A landing
bird uses its wings to decelerate the body until the feet have made contact
with the substrate, therefore, we can understand the basic mechanics of
landing for most birds by examining low-speed forward flight and deceleration
(e.g. Berg and Biewener, 2008).
However, the landings of bats cannot be understood through studies of flight
alone because bats roost head-under-heels and cannot hover in this position.
To land safely, bats perform acrobatic flips; however, while the kinematics of
flying and crawling bats have received considerable attention
(Lindhe Norberg and Winter,
2006; Rayner and Aldridge,
1985; Riskin et al.,
2005; Riskin et al.,
2006), the biomechanics of landing have essentially been
overlooked. The present study is the first to describe the three-dimensional
kinematics and kinetics of landing behaviour in bats.
Among mammals, bats have particularly slender hindlimb bones, presumably as
an adaptation for flight that decreases total body mass and shifts the center
of mass (COM) anteriorly (Swartz et al.,
2003). Slender hindlimbs, however, experience higher stresses than
robust ones would for a given load and bat hindlimbs are therefore susceptible
to high stresses when they are pressed against a surface, as they are during
walking, for example (Riskin et al.,
2005). Because bats land using their hindlimbs, they must
therefore do so in a way that keeps hindlimb bone stresses relatively small.
To land safely, a bat must bring its body into contact with an overhead
surface but without hitting the surface so hard as to suffer injury from
impact forces. A trajectory that keeps the bat further from the landing
surface decreases the risk of hindlimb injury but could result in free-fall
instead of reaching the intended landing site.
The ability to land head-under-heels has allowed bats to use a vast array
of roost types worldwide. Most of the world's >1200 bat species perform
this behaviour several times each day and bats have been doing so at least
since their first appearance in the fossil record over 50 million years ago
(Simmons et al., 2008). In the
present study, we sought to accurately describe the kinematics of landing
behaviour and to determine whether landing kinematics differ among species.
Also, we measured the impact forces during landing, to reveal potential links
between kinematics and impact forces that result during landing.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Campbell et al., 2006;
Tan et al., 1997) whereas the
other two species typically roost in caves
(Alvarez et al., 1991;
Cloutier and Thomas, 1992;
Fleming, 1988). Bats of all
three species hang head-down by their toes from their roosts. For the present
study, we used bats that had been raised in captivity and were housed at the
Concord Field Station of Harvard University (Bedford, MA, USA) (C.
brachyotis) and at the University of Maryland (College Park, MD, USA)
(C. perspicillata and G. soricina).
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Experiments were performed in flight enclosures measuring 8.3 mx1.0 mx2.4 m (LxWxH) for C. brachyotis and 1.6 mx1.3 mx2.3 m (LxWxH) for the other two species. The highest point in each enclosure was the horizontal surface of a ceiling-mounted force-measuring platform, where landings were recorded in our experiments. To discourage bats from landing in locations other than the force platform, we covered other parts of the ceiling with plastic sheets and cardboard.
For training, a bat was introduced to the enclosure and allowed to fly freely for several minutes. When it landed on a part of the enclosure other than the surface of the force platform, we gently touched it to encourage flight or captured it and placed it on the plate surface. This was repeated until the bat ended a free flight by landing on the force platform. As a general rule, once a bat landed a single time on the force platform, and was subsequently left there for a few minutes, it returned to that site after almost every flight. Training required 3–4 daily sessions for C. brachyotis and a single training session lasting 10–30 min for the other two species.
Kinematics and Euler rotation sequences
We recorded 11, 10 and eight landings from each of three individuals of
C. brachyotis and 10 landings each for five individuals of G.
soricina and five individuals of C. perspicillata. Landings were
recorded at 250 or 1000 Hz with three phase-locked Photron 1024 PCI digital
high-speed cameras (Photron USA, San Diego, CA, USA). Three-dimensional
reconstructions from camera images were performed using the Direct Linear
Transformation method (Hedrick et al.,
2004), based on a 0.35x0.35x0.28 m
(LxWxH), 40-point calibration cube held adjacent to the surface of
the force plate immediately before experiments were performed.
For each landing, we determined the time of peak impact force from the
force plate recordings (see below). We referred to this time as t=0
and aligned all other events relative to this time. For this experiment, we
were not concerned with the time varying motions of different parts of the
body but with the overall changes in the orientation of the body itself over
time. For this reason, we did not follow a specific set of kinematic markers
throughout the landing sequences, as is typically done in kinematics studies
(Riskin et al., 2008).
Instead, we measured the orientation of the bat relative to the ceiling at 11
time steps, from –0.2 s to 0.2 s, using a right-handed body-referenced
coordinate system (xb, yb,
zb) and a right-handed global coordinate system
(xg, yg, zg).
The body-referenced coordinate system moved with the bat. At each time step, we measured the position of the base of the skull and the position of the torso between the legs; xb was defined as the line through those points, with positive xb toward the head. We measured two positions on opposite sides of the body (left and right points) and defined the yb axis as the projection of this line onto the plane normal to xb, with positive yb to the bat's right. The zb axis pointed ventrally and was defined as the cross product of xb and yb. The global reference frame consisted of xg and yg in the plane orthogonal to gravity, with xg lined up with the horizontal projection of the initial xb value of the trial (0.2 s before peak impact). We defined zg as vertical, positive down.
We used different anatomical landmarks for the sides of the body over the course of a landing sequence because bats approached the ceiling with time-varying body postures that obscured almost any given anatomical location from view for at least part of the approach. When possible, we used the wingtips or wrists of the symmetrically outstretched wings. In frames where the wings were not easily digitized or the wings were not held symmetrically, we used the sides of the rib cage as left and right points. We tested whether the use of wingtips or ribs influenced our measured angles (when wings were symmetrical) and found no significant effect.
We describe the orientation of the bat at each time step relative to the
global reference frame in terms of a three-part Euler axis rotation sequence,
consisting of the pitch angle (
), yaw angle (
) and roll angle
(
) required to align the (xg, yg,
zg) with the (xb,
yb, zb). For most readers, it will be
sufficient to note that for a bat flying with its ventral surface facing
downward, a positive pitch causes the head to be raised above the feet, a
positive yaw causes the head to turn to the right and a positive roll causes
the right wing to drop and the left wing to rise. For the detail-minded
reader, pitch angle () is the rotation angle around
yg required to line zg up with the
projection of zb onto the
xg–zg plane. After the global
frame is rotated through , it occupies a new orientation
(xg', yg',
zg'). Yaw angle () is defined as the angle
around zg' required to align
xg' with xb. After the
(xg', yg',
zg') frame is rotated through , it occupies a
new orientation (xg'', yg'',
zg''). The roll angle () is defined as the angle
around xg'' necessary to align (xg'',
yg'', zg'') with
(xb, yb, zb).
The values of , and will differ depending on the order
in which they are calculated but when all three are reported, along with the
order in which they were calculated, their result is unambiguous.
Traditionally, these values are calculated in the order , , then
(Stengel, 2004).
However, this order resulted in discontinuities in our measured angles. We
therefore used the sequence order outlined above (, , then
).
Design, calibration and use of the force platform
To record the magnitudes and orientations of ceiling reaction forces during
landing, we used a custom-built force-measuring platform. Its surface
consisted of a stiff 0.28 mx0.28 m honeycombed fiberfoam surface with a
0.12 mx0.12 m area of plastic webbing at its center. Bats were unable to
grasp the flat surface of the fiberfoam so, instead, all bats landed by
grabbing the central webbing. This arrangement prevented bats from using the
edges of the platform or making contact with features of the ceiling adjacent
to the platform when landing. The webbing was also stiff and glued to the
surface to minimize the dampening of impulses that passed through it during a
landing event.
The force platform measured forces in all three dimensions and was
constructed and calibrated in the same manner as in previous studies
(Riskin et al., 2005;
Riskin et al., 2006). The
platform had resonant frequencies >290 Hz in all three directions. On days
in which landings were recorded, the force–voltage relationship of each
channel was calibrated by suspending weights (10 g–200 g) directly from
the surface or through a series of pulleys so as to apply forces in different
directions. A separate linear force-to-voltage regression slope was calculated
for forces into the ceiling, down from the ceiling and in four horizontal
directions at 90 deg. intervals. The platform demonstrated linear
force–voltage relationships in each of these six directions
(R2>0.999). Electronic drift in the baseline output was
corrected in each trial by sampling the signal of the unloaded force plate for
several seconds immediately before a landing event.
For each landing, we recorded forces at 1000 Hz and synchronized force plate recordings with videos by recording the camera trigger signal alongside the force plate's voltage signals. All forces were scaled to the body weight of the individual that produced them and are reported in units of body weights.
Force profile descriptions
The force profiles associated with landing events were similar for all
trials (see Results) and several descriptive parameters could be
systematically recorded from them. In each trial, a landing bat first struck
the ceiling, imparting a three-dimensional force to the plate that included an
upwards vertical component. We designate the total magnitude of this force in
three dimensions (Fpeak-up) and define
peak-up as its angle from vertical up (negative
zg). Next, as a result of the ceiling reaction force plus
gravity, the bat's COM began to move away from the ceiling and this separation
from the ceiling was arrested when the attached limbs were placed in tension,
causing another local peak in the net force vector, this time with its
vertical component directed downward. We refer to the magnitude of total force
at this time as Fpeak-down and define
peak-down as its angle from vertical down (positive
zg). Afterward, the vertical component of the ceiling
reaction force oscillated near –1 body weights as the bat hung from the
ceiling.
Statistical analyses
Values of body pitch that were recorded for the body at the beginning of
the approach (t=–0.2 s) were compared among species using an
analysis of variance (ANOVA) with post-hoc pairwise t-tests.
Fpeak-up and Fpeak-down values were not
normally distributed, thus, we used statistical procedures that are robust
against deviations from normality. To determine whether each of these differed
among species, we used one-way ANOVA tests on rank-transformed values for all
129 landings [i.e. Kruskal–Wallis tests
(Zar, 1999)].
Post-hoc pairwise comparisons were made using t-tests of the
rank-transformed data (Mann–Whitney U-tests). To avoid
pseudoreplication for the ANOVAs, we used two degrees of freedom (number of
species – 1) in the numerator and 12 degrees of freedom (number of
individuals – 1) in the denominator and similarly adjusted the degrees
of freedom to reflect the number of individuals in each post-hoc
comparison.
Signal filtering
We improved the signal-to-noise ratio of the force plate signals by
filtering them with a 100 Hz low-pass Butterworth filter. However, even after
filtering, oscillations in voltage due to background noise alone (an unloaded
plate) were equivalent to voltage changes that would result from ca.
0.04 N of force, around 40% of the weight of our smallest bats. This noise may
have prevented the resolution of small-magnitude impact forces, as any rapidly
applied force smaller than ca. 0.04 N would be masked by electrical
noise. Because forces were scaled to the weight of the organisms, this issue
could have potentially led to the false conclusion that small-bodied animals
produce larger peak forces than large-bodied ones when, in fact, all organisms
simply applied equivalent forces (in units of body weights) but noise
concealed the peak for small bats. One way to further decrease the magnitude
of the electrical noise would be the use of a lower (<100 Hz) Butterworth
low-pass cutoff frequency; however, stronger filtering of this kind has the
additional effect of decreasing the apparent magnitudes of the brief force
peaks associated with landing – the very peaks we sought to measure in
the present study. Thus, we used the 100 Hz cutoff frequency but to ensure
that the statistical trends we report are not artifacts of this choice, we
repeated our analyses using Butterworth low-pass filter cutoff frequencies of
50 Hz, 25 Hz and 10 Hz and using unfiltered data.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Four-point landings
In a four-point landing, a bat arrived at the ceiling with the wings
partially folded, the forelimbs extended laterally and anteriorly and the
hindlimbs extended laterally and caudally from the body
(Fig. 1A) (t=0.00 s).
After making contact with the ceiling, the bat dragged the thumbs and toes
toward the body, across the ceiling, until the claws of one or more limbs had
interlocked with a part of the surface webbing
(Fig. 1A) (t=0.04 s).
Thereafter, the bat suspended itself by the limbs that grasped the ceiling.
The four-point landing ended with a ventral belly-up posture. Subsequently,
the bat let go with its thumbs to assume a typical, head-down roosting
posture.
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Two-point landings
Individual bats performing a two-point landing did so by moving the left
and right sides of their bodies asymmetrically. These bats either brought
their hindlimbs anteriorly along the right side of their body (which we refer
to as right-handed two-point landing) (Fig.
1B,D) or along the left side of the body (left-handed two-point
landing) (Fig. 1C,E). Some
individuals alternated between right-handed and left-handed landings whereas
others consistently used one landing type; the five C. perspicillata
individuals used right-handed landings in 3/10, 4/10, 7/10, 9/10 and 9/10
trials and the five G. soricina individuals used right-handed
landings in 0/10, 0/10, 3/10, 4/10 and 8/10 trials.
For eight of the 100 two-point landings, we were unable to accurately measure Euler rotation angles because the bat was not visible in two cameras at t=–0.2 s (one trial), because of camera problems that caused the field of view to be too dark (three trials), or because of coincidental alignment of body axes with global ones during the landing sequence that interfered with the accuracy of our calculations (four trials). Video recordings of these landings were similar to the other two-point landings but these trials were omitted from our summaries of Euler rotation angles.
For two-point landings, body pitch angles at t=–0.2 s were 54.7±12.5 deg. (N=45) for C. perspicillata and 48.6±8.5 deg. (N=47) for G. soricina. These values were similar to those of C. brachyotis that used four-point landings (59.8±9.7 deg.) but were slightly lower (ANOVA: F=10.7, d.f.=2,7, P=0.002). Body yaw was zero (by definition) and, like those of bats that used four-point landings, the body roll angles were near zero (C. perspicillata, 1.5±19.0 deg.; G. soricina, 0.64±11.1 deg.).
In a right-handed two-point landing (Fig. 2B,F), body pitch increased first, then continued to increase while the body began a negative yaw rotation, bringing the feet up next to the right side of the body. Yaw rotation continued until the feet were above the head (ca. –180 deg.) and was accompanied by a slight negative body roll. The result of these rotations was that at the end of the landing sequence, bats hung from the force platform by their hindlimbs with their ventral surfaces (zb) facing toward negative yg (Fig. 3B). Left-handed two-point landings (Fig. 2C,G) were similar to right-handed ones but with the pitch and roll values changing in the opposite direction (both positive), resulting in final head-down roosting postures with the ventral surfaces (zb) oriented toward positive yg. In some landings, only one foot attached during the landing sequence and some time later, the second foot became interlocked with the ceiling. In most two-point landings, the bat swung from side-to-side for several seconds after landing. We did not observe swinging of this kind with four-point landings.
Some two-point landings did not fit the typical pattern of pitch, roll and yaw changes, even though their kinematics were very similar to those of typical two-point landings. Most plots of pitch, roll and yaw (Fig. 2) were easily assigned to left-handed, right-handed or four-point categories. However, 10 of the 45 plots for C. perspicillata revealed an alternative pattern that did not conform to any of these three categories (Fig. 2D,E). The kinematics of the 10 alternative landings were very similar to typical two-point landings but with the change in yaw initiated later. In these situations, changes in pitch throughout the landing sequence were larger and changes in yaw were smaller than in typical two-point landings. As in typical two-point landings, this alternative landing strategy resulted in a head-down roosting posture with the body facing in the same direction, as it would have in a typical landing event. This alternative landing strategy was performed by three individuals, all of which also performed typical two-point landings. We interpreted the alternative landing strategy as a variant of the typical two-point landing and did not assign it to a different category because it was almost indistinguishable from typical two-point landings in the videos.
Ceiling reaction forces
When a bat landed on the ceiling, regardless of kinematic category, there
was an initial peak in vertical force associated with the first impact of the
body with the ceiling. As the ceiling began to support the bat's weight, a
second peak in force occurred with a vertical component directed away from the
ceiling. After landing, C. perspicillata and G. soricina
swung back and forth by their toes, causing periodic oscillations in ceiling
reaction forces (Fig. 4).
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peak-up values of C.
perspicillata (20.9±73.1 deg.) or G. soricina
(24.2±26.2 deg.). Values of peak-down averaged
16.0±12.9 deg. for C. brachyotis, 49.4±23.8 deg. for
G. soricina and 51.0±46.8 deg. for C.
perspicillata.
Filtering artifacts
As expected, using lower filter cutoff frequencies decreased the apparent
magnitudes of peak forces. For example, Fpeak-up for C.
brachyotis was 3.7±2.4 body weights (median ± interquartile
range) when a 100 Hz cutoff frequency was used but only 2.9±1.5 body
weights when a 25 Hz cutoff frequency was used or 6.4±7.5 body weights
when unfiltered data were used. The lower the cutoff frequency used, the
smaller the apparent force peaks. However, the pattern of significant
differences among our statistical tests was the same for unfiltered data and
at all Butterworth low-pass cutoff frequencies used: 100 Hz, 50 Hz, 25 Hz and
10 Hz. As excess filtering would diminish the magnitudes of peak forces
relative to their actual values and because 100 Hz is a commonly used cutoff
frequency for kinematics studies, we have chosen to report the 100 Hz-filtered
data. We caution, therefore, that the actual magnitudes of peak impact force
are influenced by our filtering protocols and thus emphasize that it is the
relative difference in peak impact force among species that is of most
value.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Explaining interspecific variability in landing strategy
It is plausible that the differences in impact force that we observed among
species reflect a larger pattern among species associated with roosting
habits, wherein cave-roosting bats land more gently than foliage-roosting
taxa. A surface such as foliage that bends in response to a landing bat can
absorb impact energy and dissipate it slowly therefore the time course over
which landing forces are transmitted through the skeleton is increased,
thereby reducing peak forces and stresses. This hypothesis is supported by the
observation that the cave-roosting bats in our study landed more gently (with
smaller peak impact forces) than foliage-roosting bats did.
Alternatively, differences in landing style might be an artifact of
phylogeny; our four-point landing species is a pteropodid (Suborder
Yinpterochiroptera, formerly Megachiroptera) and the other two species are
phyllostomids [Yangochiroptera, formerly Microchiroptera
(Teeling et al., 2005)].
Differences in thumb-use during feeding between these groups have been
documented previously (Vandoros and
Dumont, 2004), so differences between them in the use of thumbs
during landing is perhaps not surprising. The vast majority of pteropodids are
foliage roosters but yangochiropterans use a diverse array of roost types
(Kunz, 1982). Resolution of
the relative influences of phylogeny and roosting ecology on landing
performance would therefore require investigation of landing performance in a
more disparate and much larger group of bat species than that presented in the
current study.
At first glance, a third possible explanation for our results would be that bats larger than ca. 25 g employ a four-point strategy and smaller bats use a two-point one. However, high-speed videos of five Artibeus jamaicensis, a cave-roosting phyllostomid similar in body mass to C. brachyotis (38.1±1.7 g; D.K.R. and J.M.R., unpublished data), revealed that, like the smaller bat species in the present study, A. jamaicensis perform a two-point landing that results in relatively small impact forces (ca. 0.3 body weights, N=1). Body size is therefore not the sole determinant of landing strategy.
Hindlimb stresses during landing
It is not surprising that for bats performing two-point landings, peak
impact forces were small as all force was transmitted to the ceiling through
the hindlimbs. Because the diameters of the hindlimb bones of bats are reduced
compared with those of terrestrial mammals, bat hindlimb long bones are better
able to accommodate tensile loading than compression or bending
(Riskin et al., 2005). The
hindlimbs of landing bats are most probably at their greatest risk of
mechanical failure at t=0.00, when peak force is applied into the
ceiling. Bats that make two-point landings are therefore required to land
gently.
We were unable to measure hindlimb stresses directly because both hindlimbs (two-point landings) or all four limbs (four-point landings) contacted the ceiling together, masking the relative contributions of each limb. Bats landing with their wrists and hindlimbs simultaneously might be able to afford larger impact forces by applying the majority of the force with their forelimbs. Based on our examination of the high-speed videos, the hindlimbs appear to strike the ceiling with considerable momentum but we cannot adequately compare hindlimb stresses between four-point and two-point landing bats with the data we collected.
Aeromechanics of landing
Immediately before landing, a bat's body has both translational momentum
and rotational momentum that will together bring the claws in contact with the
ceiling. During landing, a bat must stop both the rotation and translation of
its body using some combination of gravitational forces, ceiling reaction
forces and aerodynamic forces. Although a great deal could be learned by
quantifying the relative contributions of these forces to changes in
translational and rotational momentum, there are too many unknowns for that
accounting to be performed at present.
First, the location of the COM is difficult to calculate, owing to the
changing body posture throughout the landing sequence. Without knowledge of
its position and of the body's moment of inertia around its axes of rotation,
the translational momentum of the COM and rotational momentum of the body
around the COM cannot be computed. Second, quantification of aerodynamic
forces is even more daunting. These would need to be inferred using
computational fluid dynamics models based on wing kinematics and this is most
likely to be near the limit of the abilities of the most modern computational
methods (Mittal and Iaccarino,
2005). Moreover, the ceiling would cause wall effects
(unfortunately named in this case) that introduce solid–fluid
interactions, which further complicate the use of such models.
Ecological implications of landing performance
The implications of mid-flight manoeuvrability for feeding ecology are
obvious. For example, differences in turning ability influence the kinds of
environments in which all bats can forage for food, and insectivorous bats
must be able to make the tight turns necessary for intercepting prey
(Ghose and Moss, 2006;
Ghose et al., 2006;
Triblehorn et al., 2008). If
landing performance is considered to be a component of aerial manoeuvrability,
our results expand the implications of flight performance to include roosting
ecology as well.
The mastery of landing upside down by bats has permitted their exploitation
of an extremely diverse assemblage of roost types. Bats roost in caves and
tree hollows, under bark, against leaves, among branches and in human-made
structures, to name a few (Fenton et al.,
2001; Fenton et al.,
2000; Kunz, 1982;
Kunz and Lumsden, 2003;
Riskin and Fenton, 2001;
Riskin and Pybus, 1998).
Although a generalized landing strategy could permit bats to land on any
substrate, our results indicate that there are species-specific differences
that may make different kinds of roosts accessible to different species. In a
broader survey, we might expect to find a correlation between foraging habitat
and roost type and a complementary correlation between flight performance and
landing mechanics. Conversely, the biomechanics of landing and steady flight
might interfere with one another and result in species-specific trade-offs
that ultimately have influenced the evolutionary ecology of foraging behaviour
and roost use.
Because terrestrial locomotion results in mechanical loading of the
hindlimbs, we might also find a correlation between landing kinetics and
locomotor performance, with terrestrially agile bats such as Desmodus
tumidirostris or Mystacina parnellii able to withstand greater
compressive stresses during landing than those that cannot walk well such as
Natalus rotundus or Pteronotus tuberculata
(Riskin and Hermanson, 2005;
Riskin et al., 2005;
Riskin et al., 2006).
Vaughan noted correlations between flight performance and roost type among
bats and considered these in the context of flight initiation
(Vaughan, 1959). Our discovery
that the kinematics and kinetics of landing can vary among species adds
another dimension to the link between flight performance and roosting ecology.
Bats that can land gently at a small target might have a competitive advantage
over other bats for roosting on hard or sharp roost surfaces such as the
ceilings of caves.
Landing performance and the evolution of flight
The ability to land safely at the end of a flight is a functional
constraint on locomotor performance for any flying vertebrate. Because nearly
all bats hang head down, it appears that the ability to land at an overhead
roost has been conserved since the appearance of bats over 50 million years
ago (Jepsen, 1966;
Simmons et al., 2008;
Teeling et al., 2005). Our
results demonstrate that there are interspecific differences among bat species
in the kinematics and kinetics of landing. Future investigation of the way in
which bats end their flights will shed new light on the evolution of flight
manoeuvrability and roosting ecology in the Chiroptera.
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Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Alvarez, J., Willig, M. R., Jones, J. K., Jr and Webster, W. D. (1991). Glossophaga soricina. Mamm. Species 379,1 -7.
Berg, A. M. and Biewener, A. A. (2008).
Kinematics and power requirements of ascending and descending flight in the
pigeon (Columba livia). J. Exp. Biol.
211,1120
-1130.
Boon, P. P. and Corlett, R. T. (1989). Seed dispersal by the lesser short-nosed fruit bat (Cynopterus brachyotis, Pteropodidae, Megachiroptera). Malay. Nat. J. 42,251 -256.
Campbell, P., Reid, N. M., Zubaid, A., Adnan, A. M. and Kunz, T. H. (2006). Comparatice roosting ecology of Cynopterus (Chiroptera: Pteropodidae) fruit bats in peninsular Malaysia. Biotropica 38,725 -734.[CrossRef]
Cloutier, D. and Thomas, D. W. (1992). Carollia perspicillata. Mamm. Species 417, 1-9.
Crawford, R. L. and Baker, W. W. (1981). Bats killed at a North Florida television tower: a 25-year record. J. Mammal. 62,651 -652.[CrossRef]
Fenton, M. B., Vonhof, M. J., Bouchard, S., Gill, S. A., Johnston, D. S., Reid, F. A., Riskin, D. K., Standing, K. L., Taylor, J. R. and Wagner, R. (2000). Roosts used by Sturnira lilium (Chiroptera: Phyllostomidae) in Belize. Biotropica 32,729 -733.[CrossRef]
Fenton, M. B., Bernard, E., Bouchard, S., Hollis, L., Johnston, D. S., Lausen, C. L., Ratcliffe, J. M., Riskin, D. K., Taylor, J. R. and Zigouris, J. (2001). The bat fauna of Lamanai, Belize: roosts and trophic roles. J. Trop. Ecol. 17,511 -524.
Fleming, T. H. (1988). The Short-tailed Fruit Bat: A Study in Plant-Animal Interactions. Chicago, IL: University of Chicago Press.
Ghose, K. and Moss, C. F. (2006). Steering by
hearing: a bat's acoustic gaze is linked to its flight motor output by a
delayed, adaptive linear law. J. Neurosci.
26,1704
-1710.
Ghose, K., Horiuchi, T. K., Krishnaprasad, P. S. and Moss, C. F. (2006). Echolocating bats use a nearly time-optimal strategy to intercept prey. PLoS Biol. 4, 865-873.
Hedrick, T. L., Usherwood, J. R. and Biewener, A. A.
(2004). Wing inertia and whole-body acceleration: an analysis of
instantaneous aerodynamic force production in cockatiels (Nymphicus
hollandicus) flying across a range of speeds. J. Exp.
Biol. 207,1689
-1702.
Jepsen, G. L. (1966). Early Eocene bat from
Wyoming. Science 154,1333
-1339.
Klem, D. J. (1990). Bird injuries, cause of death, and recuperation from collisions with windows. J. Field Ornithol. 61,115 -119.
Kunz, T. H. (1982). Roosting ecology of bats. In Ecology of Bats (ed. T. H. Kunz), pp.1 -55. New York: Plenum Press.
Kunz, T. H. and Lumsden, L. F. (2003). Ecology of cavity and foliage roosting bats. In Bat Ecology (ed. T. H. Kunz and M. B. Fenton), pp. 3-89. Chicago, IL: University of Chicago Press.
Lindhe Norberg, U. M. and Winter, Y. (2006).
Wing beat kinematics of a nectar-feeding bat, Glossophaga soricina,
flying at different flight speeds and Strouhal numbers. J. Exp.
Biol. 209,3887
-3897.
Mittal, R. and Iaccarino, G. (2005). Immersed boundary methods. Annu. Rev. Fluid Mech. 37,239 -261.[CrossRef]
Rayner, J. M. V. and Aldridge, H. D. J. N.
(1985). Three-dimensional reconstruction of animal flight paths
and the turning flight of microchiropteran bats. J. Exp.
Biol. 118,247
-265.
Riskin, D. K. and Fenton, M. B. (2001). Sticking ability in Spix's disk-winged bat, Thyroptera tricolor (Microchiroptera: Thyropteridae). Can. J. Zool. 79,2261 -2267.[CrossRef]
Riskin, D. K. and Hermanson, J. W. (2005). Independent evolution of running in vampire bats. Nature 434,292 .[CrossRef][Medline]
Riskin, D. K. and Pybus, M. J. (1998). The use of exposed diurnal roosts in Alberta by the little brown bat, Myotis lucifugus. Can. J. Zool. 76,767 -770.[CrossRef]
Riskin, D. K., Bertram, J. E. A. and Hermanson, J. W.
(2005). Testing the hindlimb-strength hypothesis: non-aerial
locomotion by Chiroptera is not constrained by the dimensions of the femur or
tibia. J. Exp. Biol.
208,1309
-1319.
Riskin, D. K., Parsons, S., Schutt, W. A., Jr, Carter, G. G. and
Hermanson, J. W. (2006). Terrestrial locomotion of the New
Zealand short-tailed bat Mystacina tuberculata and the common vampire
bat Desmodus rotundus. J. Exp. Biol.
209,1725
-1736.
Riskin, D. K., Willis, D. J., Iriarte-Díaz, J., Hedrick, T. L., Kostandov, M., Chen, J., Laidlaw, D. H., Breuer, K. S. and Swartz, S. M. (2008). Quantifying the complexity of bat wing kinematics. J. Theor. Biol. 254,604 -615.[CrossRef][Medline]
Simmons, N. B., Seymour, K. L., Habersetzer, J. and Gunnell, G. F. (2008). Primitive early eocene bat from Wyoming and the evolution of flight and echolocation. Nature 451,818 -821.[CrossRef][Medline]
Stengel, R. F. (2004). Flight Dynamics. Princeton, NJ: Princeton University Press.
Swartz, S. M., Freeman, P. W. and Stockwell, E. F. (2003). Ecomorphology of bats: comparative and experimental approaches relating structural design to ecology. In Ecology of Bats (ed. T. H. Kunz and M. B. Fenton), pp.257 -300. Chicago, IL: University of Chicago Press.
Tan, K. H., Zubaid, A. and Kunz, T. H. (1997). Tent construction and social organization in Cynopterus brachyotis (Muller) (Chiroptera: Pteropodidae) in peninsular Malaysia. J. Nat. Hist. 31,1605 -1621.[CrossRef]
Teeling, E. C., Springer, M. S., Madsen, O., Bates, P., O'Brien,
S. J. and Murphy, W. J. (2005). A molecular phylogeny for
bats illuminates biogeography and the fossil record.
Science 307,580
-584.
Triblehorn, J. D., Ghose, K., Bohn, K., Moss, C. F. and Yager,
D. D. (2008). Free-flight encounters between praying mantids
(Parasphendale agrionina) and bats (Eptesicus fuscus).
J. Exp. Biol. 211,555
-562.
Vandoros, J. D. and Dumont, E. R. (2004). Use of the wings in manipulative and suspensory behaviors during feeding by frugivorous bats. J. Exp. Zool. 301A,361 -366.
Vaughan, T. A. (1959). Functional Morphology of Three Bats: Eumops, Myotis, Macrotus, pp.1 -153. Lawrence, KS: University of Kansas/Museum of Natural History.
Zar, J. H. (1999). Biostatistical Analysis. Upper Saddle River, NJ: Prentice Hall.
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