Integrative and Comparative Biology, volume 51, number 6, pp. 991–1001
doi:10.1093/icb/icr069
SYMPOSIUM
Ecological and Biomechanical Insights into the Evolution of
Gliding in Mammals
Greg Byrnes1,* and Andrew J. Spence†
*Department of Biological Sciences, University of Cincinnati, P.O. Box 210006, Cincinnati, OH 45221-0006, USA;
†
Structure and Motion Laboratory, Royal Veterinary College, Hawkshead Lane, North Mymms,
Hertfordshire AL9 7TA, UK
From the symposium ‘‘The Biomechanics and Behavior of Gliding Flight’’ presented at the annual meeting of the Society
for Integrative and Comparative Biology, January 3–7, 2011, at Salt Lake City, Utah.
1
E-mail: [email protected]
Synopsis Gliding has evolved independently at least six times in mammals. Multiple hypotheses have been proposed to
explain the evolution of gliding. These include the evasion of predators, economical locomotion or foraging, control of
landing forces, and habitat structure. Here we use a combination of comparative methods and ecological and biomechanical data collected from free-ranging animals to evaluate these hypotheses. Our comparative data suggest that the
origins of gliding are often associated with shifts to low-quality diets including leaves and plant exudates. Further, data
from free-ranging colugos suggest that although gliding is not more energetically economical than moving through the
canopy, it is much faster, allowing shorter times of transit between foraging patches and therefore more time available to
forage in a given patch. In addition to moving quickly, gliding mammals spend only a small fraction of their overall time
engaged in locomotion, likely offsetting its high cost. Kinetic data for both take-off and landing suggest that selection on
these behaviors could also have shaped the evolution of gliding. Glides are initiated by high-velocity leaps that are
potentially effective in evading arboreal predators. Further, upon landing, the ability to control aerodynamic forces
and reduce velocity prior to impact is likely key to extending distances of leaps or glides while reducing the likelihood
of injury. It is unlikely that any one of these hypotheses exclusively explains the evolution of gliding, but by examining
gliding in multiple groups of extant animals in ecological and biomechanical contexts, new insights into the evolution of
gliding can be gained.
Introduction
Selection pressures acting on an organism’s locomotor repertoire can result in novel modes of locomotion. While some locomotor transitions have
occurred in only a few cases, such as the independent
origins of flapping flight in birds, bats, pterosaurs,
and insects, others have occurred numerous times.
Gliding for example, has evolved independently at
least thirty times in vertebrates alone and is likely
to be included in the locomotor repertoire of most
arboreal organisms (Dudley et al. 2007). In mammals, gliding has evolved at least nine times, including six extant and three extinct lineages (Mein and
Romaggi 1991; Storch et al. 1996; Meng et al. 2006),
with the earliest known fossils dating to 130 mya
(Meng et al. 2006). Further, gliding mammals are a
diverse group, including at least 60 species from
these distantly related mammalian clades (Wilson
and Reeder 1993). Despite their diversity in lineage
or form, they all exhibit a gliding lifestyle and might
therefore experience common selective pressures resulting in common themes in behavior and ecology.
This study will address those possible commonalities
and discuss them in light of several hypotheses that
have been proposed to explain the evolution of
gliding.
Several hypotheses, yet to be tested, have been
proposed to explain the evolution of gliding flight.
Animals might leap or glide between trees in response to a specific habitat structure (Emmons and
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992
Gentry 1983; Dudley and DeVries 1990; Dial et al.
2004), to avoid predators (Emmons and Gentry
1983), or to increase locomotor or foraging efficiency
(Norberg 1983; Scholey 1986; Scheibe and Robins
1998; Dial 2003; Scheibe et al. 2006). Alternatively,
gliding might have evolved as a means of minimizing
the forces associated with landing after long leaps
(Paskins et al. 2007; Byrnes et al. 2008). However,
in order to gain insight into the selective forces that
might have shaped the ability to glide, detailed study
of the locomotor behavior of free-ranging gliding
animals is necessary.
Directly addressing these hypotheses has been
hampered in two ways. First of all, an historical distinction between gliding and parachuting, in which
gliding is defined by descent angles 5458 to the horizontal (Oliver 1951), has set up an operational definition that gliding occurs in the steady-state and
that maximizing the ability to cover long distances
‘‘improves’’ performance. However, numerous examples show that gliding rarely, if ever, occurs in a
steady-state in a variety of organisms, including insects (Yanoviak et al. 2005), reptiles (McGuire and
Dudley 2005; Socha et al. 2010), and mammals
(Bishop 2006; Byrnes et al. 2008). Furthermore, in
natural settings gliding animals rarely maximize the
distance covered (Table 1). As a result, our working
definition follows Dudley et al. (2007) in that gliding
is any aerial behavior that involves active regulation
of aerodynamic forces and therefore does not include
any parachuting behaviors that are strictly passive,
with no active modulation of aerodynamic forces.
The second challenge to addressing these hypotheses
has been the ability to collect unbiased data on the
movements of gliding animals in natural habitats.
However, incorporating new technologies, including
data-logging, into traditional methods of observation
have the potential to overcome this challenge.
Therefore, the goals of this article are to use available
biomechanical and ecological data to address the numerous hypotheses proposed for the evolution of
gliding and to suggest avenues of future research
into gliding in animals.
Habitat structure
Gliding animals rely on the potential energy stored
by climbing to travel horizontal distances by air. As a
result of this dependence on the vertical dimension
of arboreal habitats to initiate glides, it is no surprise
that several hypotheses relating the structure of forested habitats to gliding have been proposed. It has
been suggested that a low density of lianas (Emmons
and Gentry 1983) or greater height of the canopy
G. Byrnes and A. J. Spence
Table 1 Mean and maximum glide distances for gliding mammals
Taxon
Mean Maximum Mass
(m)
(m)
(g)
Petaurus breviceps
20.4
42
69–150 Jackson 1999
Petaurus gracilis
29.7
60
350–450 Jackson 1999
Glaucomys sabrinus
16.4
93
93 Vernes 2001
Petaurista leucogenys
19.5
50
Galeopterus variegatus 31.4
145
References
1010 Stafford et al. 2002
41000 Byrnes et al. 2011
(Dudley and Devries 1990) could explain the worldwide pattern in the diversity of gliders. More recently, by studying patterns in the amount of free
space in the canopy in both tropical and temperate
forests, Dial et al. (2004) demonstrated that sites
with a high diversity of gliders in Asia and
Australia were characterized by greater free space in
the canopy than in the other sites studied. The
canopy-height (Dudley and DeVries 1990) and
vertical-stratification (Ando and Shiraishi 1993) hypotheses are especially attractive, given the biomechanical–ecological prediction that larger gliders
may be confined to higher strata of the canopy. If
taxa are vertically stratified by body size, as has been
shown for the flying lizard Draco (Inger 1983), it
might be expected that the tallest forests will
harbor the greatest diversity of taxa. This prediction
is supported by the greatest diversity of gliding
mammals in the Dipterocarp forests of Southeast
Asia. Although this example is intriguing, many
counter examples illustrate the complexity of this
relationship. For example, the tallest forests in the
world, the North American redwood forests, harbor
only one species of gliding mammal. Similarly, in
Australia, the greatest diversity of gliders does not
occur in the tallest forests. Therefore, in order to
test this hypothesis fully, more detailed information
about heights and structure of canopies in forests
where gliders and non-gliders are actually found is
needed.
In addition, historical information about the
structure of forests in which fossil gliders first appeared in various regions of the world would greatly
enhance our understanding of the interplay between
forest structure and the evolution of gliding. Fossils
that have been attributed to gliders have been found
through geologic time in both modern-day temperate and tropical regions (e.g., Mein 1970; Storch
et al. 1996; Meng et al. 2006) and on most continents, with the first appearance of a gliding mammal
nearly 130 mya (Meng et al. 2006). Unfortunately,
many of these discoveries have been identified solely
993
Ecology and mechanics of gliding mammals
by dentition (e.g., Black 1963; Mein 1970). However,
the difficulty of distinguishing gliding forms in the
fossil record solely from dental characters has been
well established (Thorington et al. 2005), making
their historical distribution difficult to assess. More
recently, well-preserved fossil animals with gliding
affinities have been discovered (e.g., Storch et al.
1996; Meng et al. 2006), but these belong to extinct
groups, thus giving little insight into the evolution of
extant gliders. This type of data only exists in any
form for the marsupial gliders and shows an intriguing potential correlation between the drying of the
Australian continent and concomitant opening of
forest canopies with the evolution of the three independent lineages of marsupial gliders (Archer 1984;
Jackson 1999).
Fig. 1 Angle of orientation () at landing for 267 glides by
colugos. Asterisk denotes glides ending in animals landing on
the ground (4 of 267 glides, 1.5%). Inset shows how landing
angle is calculated.
Avoidance of predators
The three-dimensional structure of arboreal habitats
could also have influences on the ability of gliders to
escape predation. Flying animals have been shown to
have lower mortality than do non-volant animals
(Pomeroy 1990). Similarly, after allowing for evolutionary history, arboreal mammals have greater
longevity than do their terrestrial counterparts
(Shattuck and Williams 2010). Being arboreal, like
flying, allows for escape in three-dimensions, increasing the variability of escape paths for these animals.
Some birds take advantage of this opportunity and
avoid predation by varying their take-off trajectory
(Bonser and Rayner 1996). Arboreal mammals could
take advantage of similar strategies and it has been
debated whether gliding could increase longevity in
flying squirrels (Holmes and Austad 1994; Stapp
1994). Furthermore, gliding mammals can leap
from arboreal perches and escape the canopy without
injury (Emmons and Gentry 1983). Gliding mammals, including flying squirrels (Essner 2002;
Scheibe et al. 2007) and colugos (Byrnes et al.
2008), and other arboreal mammals, including tree
squirrels (Essner 2002) and primates (Garber 2005;
Channon et al. 2010; Legreneur et al. 2010), are capable of leaping from the canopy at high velocity.
This ability to change velocity quickly at take-off
could be paramount for escaping predators
(Howland 1974). However, unlike non-gliding animals that often crash into the canopy of adjacent
trees after leaps to escape predators (Stern and
Goldstone 2005), gliders can make controlled landings on targeted trees (Paskins et al. 2007; Byrnes
et al. 2008). Finally, by rarely venturing to the
ground some gliding mammals might minimize risks
from terrestrial predators. Although many temperate
gliding squirrels frequently come to the ground, colugos, for example, rarely terminate glides on the ground
(only 4 of 267 glides) (Fig. 1) and thus could minimize
exposure to ground-dwelling predators.
Foraging
Diet
Diet has been shown to affect the ecology both of
gliders and non-gliders alike. Dietary variables predict many ecological traits including duration of foraging (Goldingay 1989; Comport et al. 1996) and
population density (e.g., Wasserman and Chapman
2003). It is therefore likely that selection might act
on characteristics that improve an individual’s ability
to forage efficiently. The specialized diets of many
gliders has led to the suggestion that gliding could
have evolved because of its advantage in obtaining
scattered or protein-deficient foods, such as leaves or
plant exudates, that might not have been able to be
harvested otherwise (Goldingay 2000).
Here we use comparative methods to address the
hypothesis that gliding might have evolved because
of its advantage in obtaining low-quality or scattered
resources.
To test this hypothesis, dietary variables were obtained from the literature (Appendix 1, Supplemental
Material). Diet was characterized as the most
common food resource utilized. A composite phylogeny of 169 taxa (Fig. 2) was constructed including all
gliding and closely related groups. The following
major groups were included: squirrels (Mercer and
Roth 2003), other rodents (Montgelard et al. 2002),
primates (Poux and Douzery 2004), bats (Teeling
et al. 2002), and diprotodont marsupials
994
Fig. 2 Phylogenetic reconstruction of diet in mammals. Gliding
mammals are denoted by boldface type. The tree is a composite
phylogeny of 169 mammalian taxa including the six independent
lineages of gliding mammals and their close relatives.
G. Byrnes and A. J. Spence
(Osborne et al. 2002). These groups were arranged in
the context of the higher order mammalian phylogeny (Springer et al. 2004). Polytomies were resolved
in the trees by using other phylogenetic information
(Thorington et al. 2002; Mercer and Roth 2003) or
randomly when no additional information was available. For randomly resolved polytomies, alternate
resolutions had no influence on the outcome of the
analyses.
Ecological variables were recoded as binary characters, and ancestral character states were reconstructed using parsimony with ambiguities
reconstructed
using
both
ACCTRAN
and
DELTRAN resolutions. Associations between gliding
and dietary resources were tested using a concentrated changes test (Maddison 1990). Maddison’s
(1990) concentrated changes test is a test of correlated evolution that determines whether a change in
a specific character (in this case gliding) is associated
with a specific state of a second character (diet). The
probability of observing a concentration of changes
in one state of a character is compared to the null
hypothesis that the changes are distributed randomly
on the phylogeny (Maddison 1990). Due to the large
tree, data were simulated with n ¼ 5000 in place of
using the actual changes. All analyzes were performed using MacClade 4.0 PPC (Maddison and
Maddison 2000). Significance was assessed using a
rejection level of P50.05.
Gliding originated in six independent lineages in
the phylogeny. These six origins occurred in only
three of the eight categories of diet. Gliding evolved
twice each in ancestors with folivorous, frugivorous,
and exudivorous diets. Of these, there were significant associations based on the concentrated changes
test for both exudivory (ACCTRAN P ¼ 0.011;
DELTRAN P ¼ 0.023) and folivory (ACCTRAN
P ¼ 0.026; DELTRAN P ¼ 0.049). There was not a
significant association between gliding and frugivory
(ACCTRAN P ¼ 0.268; DELTRAN P ¼ 0.321) despite
gliding having evolved twice in ancestors exhibiting
frugivory.
The results of this analysis strongly support an
hypothesis relating to foraging behavior. The significant associations between gliding and these two dietary resources support Goldingay’s (2000)
hypothesis that gliders may be able to use
poor-quality, especially protein-deficient, food resources, which are unavailable to non-gliders.
Exudates (Goldingay 1990), seeds (Koenig and
Mumme 1987), and some leaves (Kavanagh and
Lambert 1990) have been shown to be of low quality
or are widely dispersed sources of nitrogen. Some
gliders have been observed to track patches of
995
Ecology and mechanics of gliding mammals
nutrient-rich foliage over great distances (Kavanagh
and Lambert 1990), an impossible or energetically
costly strategy for non-gliders. Although there are
some non-gliding mammals, including Ledbetter’s
possum and some species of marmosets, that have
exudivorous diets, Goldingay (2000) argued that
such animals rely on dense patches of forage to utilize these resources. Although fruit is another
often-scattered dietary resource, it was not significantly associated with gliding. Fruit contains a high
content of energy, and is eaten by a wide variety
of organisms. This finding suggests gliding allows
use of low-quality, but not necessarily scattered,
sources of food.
Comparison to ballistic leapers
Without detailed information on the movement and
foraging patterns of gliders and non-gliders, it is difficult to directly test the hypothesis that gliding improves foraging efficiency. However, by using simple
models based on ballistic motion, we can estimate
the influence of the aerodynamic force produced by
gliding mammals on the distance they travel. The
velocity of a body governed by ballistic motion is
given by the equations
vx ¼ v0 cos 0
ð1Þ
and
vy ¼ v0 sin 0 gt,
ð2Þ
where v0 is the take-off velocity, 0 is the take-off
angle (assumed to be 458 to maximize ballistic
range), g is the acceleration due to gravity, and t is
time. Using animal-borne data-loggers, we have recorded the take-off and landing impulse (Byrnes
et al. 2008), glide distance (Byrnes et al. 2011), and
the height climbed to initiate glides in free-ranging
Malayan colugos (Byrnes et al., in press). Using these
data, we can determine the benefit of producing
aerodynamic force on foraging range by comparing
our data to that of a model ballistic leaper, constrained with the kinetic parameters we measured.
For every recorded glide made by a colugo, we can
model a ballistic leap with the same take-off or landing kinetics and determine the distances covered. If
we constrain take-off velocity and change in vertical
distance to equal the observed data for each glide
(Fig. 3A), glide distance exceeds leap distance in
most cases (on average by a factor of 2.5), yet in
numerous instances ballistic leaping improves range
compared to gliding. This estimate is problematic
however, because allowing vertical displacement to
be equivalent between glides and ballistic leaps
Fig. 3 Estimated distance of ballistic leaps versus distance of
glides. (A) Distances of ballistic leaps are calculated using equal
take-off velocity (from Byrnes et al. 2008) and change in altitude
(Byrnes et al., in press) from the corresponding glides.
(B) Distances of ballistic leaps are calculated using take-off and
landing velocities (Byrnes et al. 2008) equal to those from
corresponding glides. Calculations of distances of ballistic leaps
assume maximum range (458 take-off angle) in both (A) and (B).
results in landing velocities that are approximately
ten times greater for leaping, with consequently
much higher landing forces. To account for this,
we also calculated foraging distance for a second
set of kinetic parameters for our ballistic model in
which take-off velocity and landing velocity were
constrained to equal the observed data from glides.
With these more realistic values for landing velocity
in the leaping model, gliding distance was more than
20 times greater than the distance of the leap predicted from the model and the distance leapt rarely
exceeded the distance of the glide (Fig. 3B). Gliding
appears to be of benefit not only because it can increase the distance traveled by an equivalent leap but
also allows these large distances to be traveled without excessive momentum at landing (Fig. 4). Despite
traveling long distances each night, colugos spend
only minutes each day moving between the patches
in which they forage. Time itself can be a valuable
currency that shapes behavior (Dunbar and Dunbar
1988; Dunbar 1992), and by gliding, colugos, like
other gliders (Goldingay 1989; Comport et al. 1996;
Scheibe et al. 2006), minimize the time spent in locomotion. In turn, gliding might maximize time
spent acquiring resources as well as the rate at
which resources can be acquired (Charnov 1976).
996
Fig. 4 Landing impulse versus distance traveled for ballistic
leaping (gray symbols) and gliding (black symbols). Landing impulses for ballistic leaps were calculated assuming a 458 take-off
angle as well as equal take-off velocities and changes in altitudes
for glides. Landing impulse for ballistic leaping increases significantly with distance traveled, but landing impulse for gliding is
unrelated to glide distance.
Locomotor economy
The locomotor-economy hypothesis has received the
greatest attention, but measuring the potential costs
of gliding locomotion and thus its benefits over
other forms of locomotion is logistically demanding.
As a result, mathematical models have primarily been
used in previous investigations of the potential costs
of gliding (Scholey 1986; Scheibe and Robins 1998;
Dial 2003). These models compare the cost of climbing to a height necessary to glide a given horizontal
distance to the cost of using quadrupedal locomotion
to travel the same distance. The metabolic cost per
unit time associated directly with gliding has been
shown to be low in other vertebrates (Baudinette
and Schmidt-Nielson 1974; Sapir et al. 2010).
Given the low metabolic cost per unit time and the
very short intervals of time over which gliding
occurs, this direct cost of gliding should be negligible
and has generally been ignored.
These models give insight into the comparative
costs of gliding in large and small animals, but rely
on generalized estimates of locomotor behavior and
glide performance. However, two important predictions have emerged from the models. First, large
gliders must glide a much longer distance compared
to small gliders before gliding is energetically cheaper
than running. For example, Scheibe and Robins
(1998) calculated that a small glider, the North
American flying squirrel, Glaucomys volans, must
glide only 3 m compared to between 50 and 100 m
for the red giant flying squirrel, Petaurista petaurista,
(Scholey 1986; Scheibe and Robins 1998) before gliding is a cheaper mode of transport. Secondly, due to
G. Byrnes and A. J. Spence
differential scaling relationships for running and
climbing, the energetic benefit of gliding may be
greatest at intermediate body sizes (Dial 2003).
Unfortunately, few empirical studies have been conducted on the energetic cost of vertical or incline
climbing (e.g., Taylor et al. 1972; Wunder and
Morrison 1974) and there is not a predictable relationship between energetic cost, incline angle and
body size (Full and Tullis 1990), making direct comparison of the costs of climbing to launch a glide as
opposed to the costs of running a given distance
difficult. Additional study of the metabolic cost of
vertical climbing in a diverse group of taxa would
be helpful for fully understanding this relationship.
Empirical data have been added to these energetic
models but the results have been inconclusive. In a
field study of another small North American flying
squirrel, it was estimated that Glaucomys sabrinus,
must glide 10 m before gliding is cheaper than running the same horizontal distance (Scheibe et al.
2006). The comparably sized marsupial glider,
Petaurus norfolcensis, however, must glide 30 m
before gliding would be less costly (Flaherty et al.
2008). These large differences in cost-effective glide
distance could be the result of substantial differences
in the locomotor ecology of the two species. However,
these studies used empirical data from only the initial
glides after release at a trap site, making it possible the
results could also reflect differences in the escape
response of the two species. Further, it is difficult to
apply the costs to an animal’s overall energy budget
because these studies focus on single glides.
To understand the influence of gliding on the
overall energy budget of an animal, detailed study
of the locomotor behavior over an ecologically relevant interval of time is required. By using
animal-borne data-loggers, we were able to collect
detailed data on locomotor behavior for Malayan
colugos over several days (Byrnes et al. 2008,
2011). From these data, we were able to quantify
every glide and every bout of climbing leading to a
glide to determine all vertical and horizontal movements. Combining these detailed data with estimates
of the metabolic costs of horizontal (Taylor et al.
1982) and vertical (Hanna et al. 2008) movement
from scaling equations, we determined that climbing
a given distance to launch a glide was no more economical than running an equivalent distance (Byrnes
et al., in press).
The locomotor ecology of gliding mammals also
does not support the locomotor-economy hypothesis. Colugos spend only a small fraction of their daily
time budget (52%) engaged in locomotor behaviors
(Byrnes et al. 2011). Similarly, two marsupial gliders
Ecology and mechanics of gliding mammals
from independent lineages, the greater glider
(Petauroides volans) and yellow-bellied glider
(Petaurus australis) use locomotion minimally,
spending 6% (Comport et al. 1996) and 4%
(Goldingay 1989) of their daily time budget engaged
in locomotor activities, respectively. Therefore, despite the high cost of climbing, little of the overall
daily energy balance is expended for locomotion. For
example, based on the scaling of field metabolic rate
(Nagy 2005), a 1 kg colugo would be predicted to
expend 800 kJ per day. On average, colugos
expend only 12 kJ climbing each day (Byrnes et al.,
in press), only 1.5% of their estimated daily energy
expenditure. Furthermore, P. volans expends 520 kJ
per day (Foley et al. 1990). If P. volans were to move
similar distances to those of colugos, locomotor costs
would total just 2.5% of the total daily energy
budget. Therefore, locomotor economy may not
play a large role in the ecology of extant colugos
and its role in the evolution of gliding is not well
supported by data from extant species.
Despite not providing the direct energetic savings
that have been hypothesized for locomotion, gliding
is a rapid form of locomotion and thus can save
travel time, possibly indirectly influencing the
energy budget. Time itself is a pressure that can influence behavior (Dunbar and Dunbar 1988; Dunbar
1992) and by gliding, the time spent traveling between the trees used for foraging can be minimized
by colugos and other gliders (Goldingay 1989;
Comport et al. 1996; Scheibe et al. 2006). In contrast,
moving through the canopy requires negotiating the
terminal branches of trees, and this could be slow or
indirect. The velocities of other arboreal mammals
on narrow substrates are relatively slow, approaching
1 ms1 (Delciellos and Vieira 2007; Stevens 2008).
Conversely, gliding mammals can travel at velocities
up to 10 ms1 or more (Stafford et al. 2002; Scheibe
et al. 2006; Byrnes et al. 2008), thereby reducing
travel time by as much as 10-fold. Therefore, although climbing and gliding may not maximize locomotor economy, moving quickly between trees
allows for more of the active period of an animal
to be spent foraging, possibly increasing the net
energy balance.
Avoidance of injury
Gliding mammals navigate a complex and discontinuous arboreal habitat under the darkness of night.
Discontinuous arboreal substrates require precise
placement of limbs and modulation of locomotor
forces while moving tens of meters above the
ground. Falls from elevated substrates can be
997
common (Schlesinger et al. 1993) and can result in
significant injury (Schultz 1939; Jurmain 1997). As a
result, arboreality requires high levels of dynamic
and postural control. As gaps between substrate elements increase in size, many arboreal animals rely on
leaping or gliding between distant supports. When
traveling long distances, they leap from trees, glide
tens of meters, and then must land safely on the
boles of trees they are unable to visualize at take-off.
High-speed collisions with stationary objects can
prove fatal in other volant animals, including birds
(Klem 1990) and bats (Crawford and Baker 1981).
Furthermore, impacts with trees during landing are
sometimes fatal to juvenile colugos that cling to their
mothers’ abdomens during glides (G. Byrnes, personal observation). Because they travel at high-speed
while gliding, their ability to modulate aerodynamic
forces while airborne and thereby reduce velocity
prior to landing is critical for survival.
Unlike many arboreal animals, including monkeys,
birds, and tree squirrels, that often land in the compliant terminal branches of trees (Stern and
Goldstone 2005), gliding mammals land on the
rigid, large-diameter boles of trees. As a result, gliding mammals experience conflicting pressures at
take-off and landing. To maximize ballistic range,
or to escape predators, gliding mammals leap at
high velocity during take-off from their perches
(Essner 2002; Scheibe et al. 2007). Furthermore,
they accelerate under the force of gravity for much
of their glide. To land safely, however, gliders must
elicit a landing maneuver that rapidly sheds excess
velocity prior to impact.
The importance of the landing maneuver has been
recognized since naturalists’ early descriptions in
field reports (e.g., Hingston 1914). More detailed descriptions of the landing maneuver have also been
presented (Scholey 1986; Ando and Shiraishi 1993;
Stafford et al. 2002). In this maneuver, angle of
attack is increased to 4608 and the animal lands
with either just the forefeet or with all four feet simultaneously (Nachtigall 1979; Scholey 1986; Scheibe
et al. 2007), reorienting the patagial membrane to
the oncoming flow to act as a parachute reducing
velocity prior to impact.
To measure landing forces, an instrumented force
pole has been used for leaping strepsirhine primates
(Demes et al. 1995, 1999) and flying squirrels
(Paskins et al. 2007). Over leaps or glides of short
distances of up to 2.5 m, peak impact forces increase
with distance both in the southern flying squirrel
(Glaucomys volans) (Paskins et al. 2007) and in primates (Demes et al. 1995, 1999). However, once an
animal enters a steady-state glide with no net
998
acceleration, landing forces no longer increase. Using
an animal-borne accelerometry system to measure
the landing kinetics of free-ranging colugos
(Galeopterus variegatus), Byrnes et al. (2008) found
that peak landing forces decreased with increasing
length of glide for glides ranging from 2 to 145 m.
Furthermore, there is a critical length of glide up to
which landing forces drop significantly and then level
off. This glide length may correspond to the time it
takes the animal to complete the landing maneuver
and to land with all four limbs simultaneously. As a
result of this maneuver, velocity just prior to landing
is reduced by up to 60% (Byrnes et al. 2008). This
ability to slow down prior to impact is a significant
advantage to gliding animals over their leaping precursors. The ability to modulate aerodynamic forces
and reduce velocity prior to impact allows gliding
animals to travel long distances and reduce landing
impulses compared to ballistic leaping (Fig. 4). The
ability to avoid injury by implementing complex
aerodynamic control at landing likely influenced
the animals’ ability to travel longer distances by
gliding.
Conclusions and future directions
This article has discussed how examining both the
biomechanics and ecology of extant gliders can give
insights into the evolution of gliding in mammals.
Recent biomechanical studies of gliding (i.e.,
Yanoviak et al. 2005; Bishop 2006; Socha et al.
2010) have shown compelling evidence that gliding
rarely occurs in the steady-state. Further, evidence
from the locomotor ecology of gliding mammals
suggests that they glide infrequently (i.e., Comport
et al. 1996; Byrnes et al. 2011) and do not regularly
maximize the distance covered. These results should
shift our focus from the assumption that maximizing
the distance of the glide is the most important metric
of glide performance to understanding the aerodynamic control required to perform these aerial behaviors and for assessing the ecological conditions
that drive their use. In trying to apply this new
framework, we have discussed the many hypotheses
that have been suggested for the origins of gliding. It
is likely that none of these factors alone contributed
to the evolution of gliding. However, given our current understanding, hypotheses relating to foraging
have the most support thus far. Using comparative
methods, we have shown that gliding is associated
with low-quality diets. Further, using simple ballistic
models we have shown that by producing aerodynamic forces gliding mammals can forage over greater distances with equivalent effort. Although gliding
G. Byrnes and A. J. Spence
appears to be related to foraging behavior, it might
not be because gliding is an economical form of locomotion. Instead it likely saves time in traveling
and therefore allows for dependence on low-quality
or possibly scattered resources or provides more time
for acquiring resources. It is also likely that gliders,
like many arboreal animals, are able to use
high-velocity leaps to escape predators. However,
leaping at high velocity increases risks of injury
upon landing, especially when leaping long distances.
The ability to modulate aerodynamic forces during
gliding has allowed gliding animals to decouple
take-off velocities and landing velocities and simultaneously improve range. Therefore, it is likely that
the ability to modulate forces while airborne was a
key transition in the evolution of controlled gliding.
To further understand the evolution of gliding,
future research should address the following questions: (1) How do extant gliders use this form of
locomotion? and (2) Why don’t more arboreal animals glide? In other words, what are the costs associated with a gliding versus an arboreal lifestyle? To
answer the first question, it is now possible to get a
detailed glimpse of the locomotor ecology of gliders
by using a variety of newly available technologies.
We have shown the utility of using animal-borne
data loggers in our studies of both the ecology and
biomechanics of free-ranging colugos. These, or similar, methods could be used on a variety of other
gliding mammals to understand relationships between both biomechanical and ecological variables
and other factors including body size or lineage.
Further, understanding the differential costs of gliding and non-gliding lifestyles is critical to an understanding of why animals glide. For example, it has
recently been shown that flying squirrels have greater
metabolic costs while running on the level compared
to non-gliding tree squirrels (Flaherty et al. 2010).
More generally, we do not have a good understanding of the costs of arboreal locomotion compared to
terrestrial locomotion. By understanding these costs,
and combining them with detailed information
about the movements of animals in the field, we
can gain a better picture of the differential costs of
a gliding lifestyle.
Acknowledgments
We would like to thank Robert Dudley and Steve
Yanoviak for organizing this symposium and inviting
us to participate. We would also like to thank the
other participants of the symposium for their discussions of the topic. We also thank the editor and two
Ecology and mechanics of gliding mammals
999
anonymous reviewers for their comments that have
improved the article.
Demes B, Fleagle JG, Jungers WL. 1999. Take-off and landing
forces of leaping strepsirhine primates. J Hum Evol
37:279–92.
Funding
Demes B, Jungers WL, Gross TS, Fleagle JG. 1995. Kinetics of
leaping primates: influence of substrate orientation and
compliance. Am J Phys Anthropol 96:419–29.
Summer Graduate Research Fellowship from the
Department of Integrative Biology, University of
California, Berkeley and from Wildlife Reserves
Singapore (to G.B.); Royal Society International
Travel Grant (to A.J.S. and G.B.).
Supplementary Data
Supplementary data are available at ICB online.
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