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Comparative locomotor ecology of gibbons and macaques Selection of canopy elements for crossing gaps.

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Comparative Locomotor Ecology of Gibbons and Macaques:
Selection of Canopy Elements for Crossing Gaps
Department of Anthropology, Haruard Uniuersity, Cambridge,
Massachusetts 02138
Arboreal locomotion, Functional ecology, Canopy
structure, Gaps, Selectivity
To examine functional questions of arboreal locomotor ecology, the selection of canopy elements by Bornean agile gibbons (Hylobates
agilis) and long-tailed macaques (Macaca fascicularis) was contrasted, and
related to locomotor behaviors. The two species, and in some cases, the
macaque sexes, varied in their use of most structural elements. Although both
species traveled most frequently in the main canopy layer (macaques: 56%,
gibbons: 48%),the gibbons strongly preferred the emergent canopy layer and
traveled higher than the macaques (31 vs. 23 m above ground) in larger trees
(48 vs. 26 cm dbh). Macaques preferred to cross narrower gaps (50%were in
the class 0.1-0.5 m wide) than gibbons (42%were 1.6-3.0 m wide), consistent
with the maximum gap width each crossed (3.5 m for macaques, 9 m for
gibbons). Macaques could cross only 12%of the gaps encountered in the main
canopy, and < 5%of the gaps in each of the other four layers. In contrast, all
layers appear relatively continuous for gibbons. Specialized locomotor modes
were used disproportionately at the beginning and end of travel segments,
further indicating that behavior was organized around gap crossings. A model
is defined, the Perceived Continuity Index (PCI), which predicts the relative
use of canopy strata for each species, based on the percentage of gaps a species
can cross, the frequency of gaps, and median length of continuous canopy
structure in each canopy layer. The results support the hypothesis that locomotor behaviors, and strategies of selecting canopy strata for travel, are
strongly constrained by wide gaps between trees and are ultimately based on
selection for efficient direct line travel between distant points.
0 1994 Wiley-Liss, Inc.
In the Southeast Asian tropical rainforests, an incredible diversity of mammals
share the arboreal environment, using extremely varied locomotor behaviors; sympatric gliding squirrels, jumping and running primates, squirrels, rats and civets,
brachiating apes and slow clambering sun
bears all exploit canopy plant foods. The
niche separations among members of this
arboreal guild have traditionally been depicted in terms of the vertical stratification
during travel and feeding (e.g., MacKinnon,
in Whitmore, 1984). This stratification has
often been explained by differences in their
locomotor behavior. Although studies relat0 1994 WILEY-LISS, INC
ing the locomotor behavior of rainforest
mammals to their ecological niches have almost exclusively concerned primates, these
have not been designed to test functional
hypotheses about locomotor differences
among species. Research has focused on the
quantitative descriptions of frequencies and
Received January 29, 1993; accepted October 17,1993.
Address reprint requests to Dr. Mark Leighton,Departmentof
Anthropology, Harvard University, Cambridge, MA 02138.
contexts of locomotor behavior by primates
and their relative use of canopy strata and
structural supports of different sizes.
Sympatric species typically differ in their
locomotor specializations, and oRen travel
through different strata (Curtin, 1977; Morbeck, 1977; Mittermeier, 1978; Fleagle,
1978; Fleagle and Mittermeier, 1980;
MacKinnon and MacKinnon, 1980; Gittins,
1983; Crompton, 1984; Yoneda, 1984).
These studies do not test hypotheses of
niche separation, unless stratification of
travel is examined relative to the available
structure of the canopy or to the distribution
and availability of food resources. Comparative functional analyses of posture and locomotion require examining the benefits or
costs of different behaviors in a functional
(i.e., selective) context relative t o some correlate of fitness, such as feeding efficiency
(Clutton-Brock and Harvey, 1984). Such
analyses require different objectives and
methods than those of previous studies.
Attention must be given to describing the
arboreal environment itself in terms of
the problems it presents to achieving
efficient performance in travel or in feeding
(Ripley, 1967; Morbeck, 1977; Temerin
and Cant, 1983; Pounds, 1991). The variables and contexts used to describe locomotor behavior must be oriented towards testing hypotheses of solutions to these problems.
This paper examines the evolutionary
ecology of locomotor behavior through comparative analysis of the selective use of canopy strata during travel, and the constraining factors underlying this selection, by two
sympatric Bornean primate species: the agile gibbon (Hylobates agilis, hereafter gibbons) and the long-tailed macaque (Macaca
fascicularis, hereafter macaques). An analysis of locomotor behavior that focuses on
where and how efficiently mammals travel
is relevant to the functional analysis of
several problems of their evolutionary ecology, as exemplified by the insights into
ranging and feeding ecology from analyses of terrestrial quadrupeds (e.g., Pennycuick, 1979). However, the problem of
horizontal travel, of getting from point a to
b, is particularly acute for large-bodied,
arboreal primates, most of which occupy
large home ranges and travel long distances
each day.
Rainforest canopy structure and the
problems it presents for direct,
horizontal travel
Efficient travel through the rainforest
canopy, in terms of minimizing deviations
from direct travel between two points, is
constrained not only by the ability to use
available structure, but also by the ability to
cross canopy discontinuities, or gaps (Temerin and Cant, 1983; Cant, 1988). The decision of where to cross gaps not only depends on the direction of travel but also on
the availability of sufficiently narrow gaps
with appropriate structure at either end for
its typical method of crossing these gaps.
Therefore, the animal must constantly solve
the immediate problem of how to travel
through a tree crown in order to cross into
the next crown, while minimizing the deviation from directed travel towards its ultimate goal (Temerin and Cant, 1983). Given
the complexity of locomotor behavior and
the difficulty of evaluating what structure is
available ahead, this decision process involves a great number of factors, some less
predictable than others. It is not surprising
that rainforest arboreal mammals usually
stop briefly in each tree crown to choose between the travel paths available to them
(see Results).
Clearly, the animal’s perspective of the
continuity of a given canopy-the relative
number and diversity of travel paths available-varies between species, depending on
their morphological and behavioral attributes. Past research has focused on describing these latter two aspects of locomotor ecology. Several authors have discussed
the importance of demonstrating “selective”
use of canopy structure for an effective functional analysis of behavior (Ripley, 1967;
Morbeck, 1977; Mittermeier, 1978; Garber,
19841,but few have sampled both the immediate structural context of behavior and the
availability of structures, as is necessary to
demonstrate preference for a structural feature. Some researchers (Gautier-Hion et al.,
1981;Whitten, 1982; Crompton, 1984; Ganzhorn, 1989) have described forest structure
by quantifying the density of trees of differ-
ent sizes and the widths of tree crowns, but
have not linked these variables directly to
the disproportionate use of available structure. The question why primates with specific locomotor abilities might select particular canopy strata requires this link.
Testing hypotheses of selective canopy
use requires methods that quantify both the
incidence of structures available for travel
(Ripley, 1967) and the types of gaps between
trees which must be crossed (Napier, 1967).
Without these measures, it is impossible to
distinguish whether the primate uses a
structure merely because of its predominance in the environment or if it is selected
because of its structural appropriateness for
travel. If the availability of different structural components and the incidence of gaps
are measured, however, locomotor decisionmaking can be examined, and we can distinguish casual from causal interactions of behavior and structure. Further, unless the
variation in available canopy features is described, field studies completed at different
times and in different locations cannot be
compared because the structure of the canopy might vary between habitats, forest
types, or disturbance histories, confounding
their interpretation (e.g., Mittermeier, 1978;
Gittins, 1983; Boinski, 1989). So what factors affect stratum choice and how can they
be quantified?
and patterning of this mosaic is poorly understood. Is most of the forest mature, tall
and diversely layered, with small islands of
messy, successional forest, or do the patches
of less strcturally developed, building phase
forest dominate? Do corridors of well developed canopy run through adjacent younger
canopy? How does this vary between different geographic locations? Lack of knowledge
of spatial patterning of canopy structure
and successional stages complicates robust,
generalizable descriptions of canopy use.
If only the layer of travel is documented,
then travel occurring in different forest habitats or types, which are stratified similarly
but have different spatial relationships both
within and between strata, cannot be distinguished. Two sympatric species could travel
through the same piece of forest but select
different successional stages, thus selecting
different structures within each subhabitat.
The actual structural features guiding selection could be obscured, as could differences
in the use of the canopy between species.
Because even experienced individuals have
found it difficult to identify and reliably
classify successional stages, several variables should be collected in combination
with layer to provide a broad picture of canopy structure and its use (e.g., Whitten,
1982; Ganzhorn, 1989).
Height above ground has commonly been
recorded by primatologists (MacKinnon and
Methodology for examining selective
MacKinnon, 1978; Cant, 1987; Boinski,
canopy use
19891,but evaluation of its effect requires its
Most primatologists have followed the joint analysis with the structural variables.
classical profile diagram of primary, well- Variation between species in their height of
drained rainforest (Richards, 1952) in de- travel but not in their use of strata would
scribing canopy stratification (Napier, 1966; suggest that they are choosing to travel
Morbeck, 1977; Fleagle, 1978; Gittins, through differently statured portions of the
1983). Three layers, the understory, the same forest. The size of trees (its “dbh” or
main canopy, and the emergent trees, are bole diameter at breast height) is also a
distinguished as the organizing structural strong indicator of the stature and maturity
components of the canopy. The biological re- of a piece of forest. This data is readily availality of canopy stratification is based on the able and can demonstrate selection for a
“inversion surface” caused by light competi- particular forest type.
Another variable constraining travel is
tion between tree crowns. The height where
this competition occurs, and therefore the the degree of horizontal continuity between
vertical structure of the canopy, is deter- tree crowns (Napier, 1967; Ripley, 1967;
mined by the history of disturbance and re- Cant, 1987). The classical description of the
generation a t a particular site, creating a rainforest canopy suggests that horizontal
complex mosaic of different successional continuity should vary among canopy laystages (Whitmore, 1984). The spatial scale ers, providing a basis for the selection of can-
opy strata based upon their degree of continuity. By relating the horizontal continuity
between tree crowns within each strata to
detailed data on how and when the animal
crosses gaps of different widths, it would be
possible to infer the density of its potential
travel paths. If both locomotor behavior and
horizontal continuity depend on canopy
strata, then the degree of continuity could be
a powerful predictor of the strata an animal
chooses, or alternatively, to which it is confined.
All of the variables discussed above are
expected to vary among adjacent rainforest
habitats, yet the possible effect of habitat
variation has been largely ignored in previous discussions of arboreal locomotion. The
rubric of “moist tropical forest,” encompasses a diversity of distinct habitats, distinguished by forest stature, biomass, plant
species composition, and rate of natural disturbance, which in turn determines the mosaic of structural successional phases (Whitmore, 1984). In our study, quantitative
descriptions of canopy structure in each
habitat, when combined with selectivity
analysis to delineate which factors underlie
choice of travel path, enable us to address
why some species are limited to only a few
habitats while others appear in almost all
habitats available to them.
Study species
Gibbons and long-tailed macaques are
particularly appropriate for comparative
analysis (Temerin and Cant, 1983; Grand,
1984; Cant, 1992). They are sympatric primates of similar body mass and have similar
ecological relationships with food resources
and predators, but vary markedly in locomotor behavior and anatomy and in intriguing
aspects of feeding ecology and socioecology.
Although the two species are faced with the
same distribution of possible food resources
from which they choose a diet and feed on
the same gross categories of food (MacKmnon and MacKinnon, 1978; Rodman, 1978;
Gittins, 1982; von Schaik and van Noordwick, 1986; Leighton unpubl.), they have
evolved distinct solutions to the problems of
arboreal travel. Gibbons most commonly
brachiate or progress bimanually (Fleagle,
1976; Gittins, 1983). Macaques are arboreal
quadrupeds (Cant, 1988);their locomotion is
cautious and slow in contrast to the gibbons
(Grand, 1984). The similarity of their diets
may be slightly overstated because of the
great difficulty in making careful observations, macaques spending more time foraging for insects and eating more unripe fruit
(Cant, pers. comm.).
In this study, we contrast the relevant
canopy structural variables of several rainforest habitats included within the home
ranges of the single groups of macaque and
gibbon we studied, and examine how the two
species organize their travel in response to
these variables. We address the following
specific questions:
1. Are these two primate species selective
of the canopy layer in which they
2. If so, how are their preferences related
t o variables of forest structure?
3. How does each species solve the problem of crossing gaps, and do their abilities in solving this problem constrain
their use of canopy strata for travel?
4. Can the use of different locomotor behaviors be related to the problem of
crossing gaps?
5. How does the stability of limbs and
twigs relate to the diameters of structures used for travel and for crossing
gaps, and do the species and for
macaque, the sexes, select combinations of diameters and stability for
Study area and subjects
The study was conducted at the Cabang
Panti Research Station, Gunung Palung National Park, West Kalimantan, Indonesia
(1.13”S,110.7”E),20 km from the southwest
coast of Borneo (Mitani, 1990). The research
site of 15 km2 is comprised of a mosaic of
pristine rainforest formations or habitats:
peat forest, freshwater swamp, alluvial
bench forest, well-drained lowland forest on
sandstone-derived soils and submontane
forest on granite soils (Whitmore, 1984).
Riverine Forest
Fast-Draining Swamp
Slow-Draining Swamp Forest
Alluvial Bench Forest
Transnion Forest
Lowland Sandstone
Fig. 1. Map of home ranges of the gibbon (solidline) and macaque (dashed line) study groups, and the
distributions of six lowland rainforest habitats within their home ranges.
These occur over an elevational range from
approximately 20 m to 960 m. Rainfall averages about 4,500 mm per annum.
Observations were limited to one group of
each species, selected because they shared
the same home ranges within an area of diverse habitats (Fig. l), and because the
macaque group had already been habituated to human observers. Data were collected from January to June 1988 by C. Cannon. A total of 74 segments were collected
for the macaques during which they traveled 617 m in 1,883 s, while 37 segments
were collected for the gibbons, covering
262.5 m in 208 s. The majority of the data for
gibbons were obtained from May to June
1988, following a period spent habituating
the gibbons. The gibbon group consisted of
one adult pair, a subadult female, and one
infant born at the outset of this study. The
macaque group consisted of three adult females, one adult male, one subadult female,
one subadult male, several adolescents, and
one infant carried by its mother. Only adults
were used as study subjects to minimize the
effects of body size.
Travel observations
The sampling unit for these observations
was a complete segment of locomotion,
which began when movement was initiated
from a resting posture and ended when
movement stopped and the animal returned
to a resting posture. This definition of a
“segment” of travel here should be distinguished from that used commonly by Fleagle (1976) and other primatologists. In this
study, segments of travel, and not specific
locomotor patterns, were the focus of sampling. If the individual stopped or diverted
movement to forage for insects or to interact
with another individual, the segment was
not included. This sampling unit was
adopted to investigate locomotor strategy as
a sequence of locomotor behaviors and to
measure the rate and directness of travel
(Cannon and Leighton, in prep.).
The majority of the observations recorded
were collected during morning followings
typically lasting six hours, from sunup to
midday. The same species was not sampled
on consecutive days. Individual adults were
sampled opportunistically as travel could be
observed, but observations were rotated
among the adults. Rotation was difficult for
gibbons because they would often forage individually; therefore, one individual might
be followed for up to a n hour before switching. No samples were taken within fifteen
minutes of each other to allow consecutive
samples to be reasonably independent. A
sample had to meet three criteria to be included: (1)the individual observed must be
targeted before movement and therefore before sampling began, (2) the entire segment
of travel must be observed, and (3)the end of
the segment must be observed. The first criterion avoided focusing on extraordinary
eye-catching activities. The second ensured
that even brief, possibly critical transitional
behaviors were sampled. The third insured
that we sampled only “complete” segments
of locomotion.
These requirements could possibly have
biased observation towards shorter segments, but very few (< 5%)were thrown out
because of a n inability to follow the individual’s movement. Most segments were rejected because the individual stopped to forage for insects or reacted to the observer. A
microcassette recorder and a stopwatch
were used to collect observations for the gibbons, but this was unnecessary for the
macaques because of their slow rate of travel
and limited gymnastic repertoire. All observations were limited to locomotion occurring
in the course of travel between feeding locations, with special attention paid to crossings between tree crowns. The individual
was identified by sex, and if female, whether
or not she carried a n infant.
The variables collected for each segment
concerned locomotor behavior and the structural context of travel. Variables describing
the structural context of travel included
habitat type and four measures of vertical
stratification: (1) canopy layer, ( 2 ) height
above ground (HAG) estimated t o the nearest meter, (3) distance to the most continuous stratum located directly above or below
the traveling subject (measured to the nearest meter), and (4)diameter at breast height
(dbh) of the tree in which travel ended (estimated to the nearest cm at 137 cm above
ground). Travel supports were characterized
by their: (1)diameter, estimated to the nearest cm, (2) angle of orientation relative to the
horizontal, estimated to the nearest ten degrees, and (3) stability (see Morbeck, 1977).
Support stability refers to the flexibility of a
structural support when used by a n animal
and was not the inherent, mechanical stability of the support. Stability was classified by
whether the support: (1)was stable (did not
move), (2) moved very slightly, (3) moved
> 5 cm and G 0.25 m, (4)moved > 0.25 and
s 0.5 m, (5) moved > 0.5 and s 1m and (6)
moved > 1 m. The width of crossings between tree crowns was defined as the gaps
between available woody structure he.,
from twig to twig, not leaf to leaf), estimated
to the nearest 0.5 m. All distance and support size estimates were made using the average length of a gibbon or macaque torso as
a relative guide. Estimates of gap widths,
support diameters, or support deformations
were made while the subject used them or
immediately thereafter.
If the focal individual crossed between
trees during a segment, the mode of locomotion used was noted. In order to bolster sample sizes, additional crossings were opportunistically sampled, following the three
criteria for selecting unbiased samples described above. A total of 83 crossings were
observed for the macaques and 49 crossings
for the gibbons.
Locomotor behavior was described by the
mode of locomotion and the distance traveled, to the nearest 0.5 m, while the mode
was continuously used. The locomotor
modes employed by the two species follow
definitions used by previous workers (Cant,
1988; Fleagle, 1976). Leaping is discontinuous progression, the hindlimbs providing all
propulsion. Bipedal walking is continuous,
using the hindlimbs with the torso erect.
Quadrupedalism is continuous, with all four
limbs used below the body. Brachiation (arm
swinging) is discontinuous progression in
which the forelimbs are used in a suspended
posture. Scrambling is irregular progression
across more than one support, with a variety
of limbs and postures being used, including
pronograde clambering (Cant, 1987). Climbing is continuous progression up or down an
approximately vertical support. Bridging is
a cautious, discontinuous progression, in
which the individual reaches across the distance between supports while remaining anchored on the original support and transferring weight across the gap. Macaques do this
forelimbs first, whereas gibbons generally
bridge hindlimbs first. Hopping is discontinuous progression using both hindlimbs and
forelimbs equally for the propulsive force. A
behavior classified as “stepping” was included for gibbons. Often during rapid sequences of brachiation, the individual would
step on a support with a hindlimb, bouncing
between two supports too wide for normal
brachiation. We did not feel this qualified as
bipedalism nor should it be included under
The sequence in which the modes occurred in each sample was recorded; each
mode was assigned to one of five classes according to its place in the segment: the first,
the second, the middle, the second to last,
and the last. Segments of only one mode
were placed in the first position. If two
modes were used in a segment, they were
assigned to the first and the last; if three, to
the first, middle, and last; if four, to the
first, second, middle, and last.
quarter method (Mueller-Dombois and Ellenberg, 1977). At 25 m intervals along the
transect (5 points per transect, 60 lines total), a 20 m line was laid perpendicular to
the transect on alternating sides of the
transect. At 5 m intervals along this line (5
points per line, 300 points total), vertical
structure was sampled. The method had to
be modified to sample the riverine habitat,
which runs along the Air Putih stream. The
starting points for each of two 250 m
transects, running along each side river,
were randomly selected and moved 20
meters away from the river’s edge. The
transect then followed the river’s course.
The distance to the nearest tree was measured only in the two quadrants away from
the river. The perpendicular lines were run
every 50 m.
The two variables measured using the
point-centered quarter method were the distance of the nearest tree from the sample
point and the tree’s size (dbh). Variables of
vertical structure included the presence or
absence of each of five canopy layers and,
when present, visually estimating their
height above ground and thickness (depth)
to the nearest m. Five canopy layers were
identified: (1)the understory, which is generally discontinuous horizontally and is discontinuous vertically from the main canopy
above; ( 2 ) the low canopy, defined as the
bottommost branches of the main canopy
Sampling canopy structure
trees, which is often discontinuous horizonTo collect measures of the frequency of tally and can be characterized by negatively
structural features of forest, twelve 100 m inclined branches and twigs; ( 3 ) the main
transects were laid out within the home canopy, which is relatively discontinuous
ranges of the two study groups, two in each horizontally and consists of a wide variety of
of the following habitat types: (1)riverine branch sizes and inclinations; (4) the high
forest, ( 2 ) fast-draining alluvial swamp, ( 3 ) canopy, defined as the topmost branches of
slow-draining bench swamp, (4) alluvial the main canopy trees, which are often disbench forest, (5) transition forest between continuous horizontally, and can be characslow-draining swamp and alluvial bench, terized by branches and twigs with high posand (6) lowland sandstone forest. The loca- itive inclinations; and (5) the emergent
tion and direction of each transect was de- layers, which are very large individual trees
termined in a stratified random fashion, that rise above the rest of the canopy and are
with the restriction that the transect had to often discontinuous horizontally and vertiremain entirely within the habitat type and cally.
The line-intercept method was used to
within the home ranges of both study
groups. At 50 m intervals along each measure horizontal continuity a t each of the
transect ( 3 points per transect, 36 points to- five points along the perpendiculars to the
tal), the distance to the nearest tree > 10 cm main transects. The variable of continuity
was measured, using the point-centered was the width of gaps (to the nearest 0.1 m)
between tree crowns for each of the five can- collapsed into a 2 x 2 table for each class, so
opy layers. These gaps were measured by that the significant differences, between dislaying a measuring tape along the perpen- tributions could be identified, using the
dicular and using a clinometer to insure pre- equation of Ynetta (pers. comm.):
cise vertical projection; either end of the gap x2ij = [(Eij - O i j ) ' ~ i j ~ / [ ( l - ( C i ~ ) ) ~ ( l - ( R j ~ ) ) l ;
was estimated on the tape. These gaps were where E, is the expected and 0, the actual
defined to extend between the smallest sup- number of observations, Ci is the total numports used during crossings and not 'foliage' ber of observations in the ith column, % is
gaps. These smallest supports used were es- the total number of observations in the jth
timated at 0.5 cm in diameter from prior row, and T is the total number of all observaobservations of travel. Occasionally, one end tions.
To examine how the three structural feaof a gap lay beyond either end of the lineintercept sample. These partial gaps were tures (layer, dbh, and distance from the
included in the data set by doubling their nearest continuous stratum) and species use
length, because they will, on average, be half of each structural feature varied with height
in and half out of all samples. This was nec- above ground, 2-factor MANOVASwere peressary to ensure that the distribution of gap formed, controlling for appropriate habitat
widths as not biased against gaps larger groups which were different in the availabilthan 10 m, which would have been included ity of the feature being examined. Only the
within the 20 m samples less than half of the upper three canopy layers were included in
time. Measures of variance become inflated the analysis for layer, and only the slowthrough this procedure, but the gap widths draining swamp, transition swamp bench,
are only analyzed by their frequency, size alluvial bench, and sandstone habitats were
included in the analyses of layer and of disdistributions and median width.
tance from the nearest continuous canopy.
Statistical methods
The index used to measure preference for
of canopy layer
different structural features is Jacob's D
value (Jacobs, 1974):
Availability by habitat
The relative availability of structure in
the five canopy layers varied among the six
where r is the relative frequency of use and p habitats (x2 = 32.4, 20 d.f., p < .05), but
is relative frequency of availability. This only two of the pairwise comparisons bevalue was chosen because it is bounded be- tween habitats were significant; the rivertween -1 and 1, is symmetrical around 0, ine habitat had structure present more frewhich indicates neutrality (neither dispro- quently in the understory and emergent
portionate selection nor avoidance) and re- layers than either the slow-draining swamp
lies directly on measures of availability (x' = 15.8, 4 d.f., p < ,051 or the alluvial
(Cock,1978). Positive values indicate prefer- bench (x2 = 14.7, 4 d.f., p < .05). The riverence while negative values indicate avoid- ine habitat was therefore excluded from the
ance. Statistical tests for significance in se- analysis of selectivity by canopy layer belectivity were by contingency table analysis cause of its distinctiveness, and because
(x'), Mann-Whitney tests, Kruskal-Wallis only six segments of travel were observed
tests, and multivariate analysis of variance there; data from the fast-draining swamp
(MANOVA; Conover, 1980). In contingency were excluded because no travel segments
analyses, classes were constructed to insure were recorded there. Availability of strucas fine-tuned an analysis as possible with- ture for travel use by canopy layer was
out violating rules for applying the test (i.e., therefore compiled from all points sampled
all expected values should be a 1.0; in the other four habitats; the main canopy
Conover, 1980). When a significant result was the most common layer (present at 82%
was obtained in a contingency table, it was of all sample points) and the understory and
D = (r-p)/(r+p-2rp),
Fig. 2. The Jacob’s D preference value for each canopy layer. The blackened symbols indicate significant
results ( p < ,051 in a 2 x 2 contingency table for that
canopy layer. Positive values indicate preference while
negative values indicate avoidance.
ground(x2 = 67.4,40d.f.,p < .Ol).Pairwise
comparisons among habitats showed that
the riverine, slow-draining swamp, and
bench habitats were similar to one another;
these were combined to form habitat group
1. The transition swamp bench and sandstone habitats had similar HAG distributions and were combined to form habitat
group 2. Habitat group 1had more structure
available at lower levels (13-20 m HAG)
than did group 2, whereas structure was
more available at 25-36 m HAG in group 2
(x2 = 26.3,8 d.f.,p < .001). Therefore, group
1 habitats have a higher frequency of structure at lower heights and lower frequency at
higher heights than group 2. As was the case
for canopy layer, sample points from the
fast-draining swamp habitat were excluded
from calculations because no travel was observed there.
the emergent layers were the least common
(both 28%presence).
Use by macaques and gibbons
Neither species traveled in the canopy
layers according to structural availability
(macaques, x2 = 14.9, 4 d.f., p < .01; gibbons, x2 = 22.5, 4 d.f., p < .001). The
macaques preferred the main canopy
(x2 = 10.27, 1 d.f.,p < .001), traveling 55%
of the time in that stratum, while neglecting
the understory (x2 = 4.95, 1 d.f., p < .05),
where only 2% of travel occurred (Fig. 2).
The gibbons completely avoided both the understory and the low canopy (x2 = 4.66, 1
d.f.,p < .05; x2 = 10.79, 1 d.f.,p < .001, respectively) and strongly preferred the emergent layer (x2 = 16.93, 1 d.f., p < .0001),
where 32% of travel occurred (Figs. 2). The
two species differed in relative canopy layer
use (Mann-Whitney test, z = 3.4, p < .001),
with macaques traveling more frequently
in low canopy (x2 = 8.94, 1 d.f., p < .01)
and gibbons more in the emergent layer
(x2 = 10.54, 1 d . f , p < .001; Fig. 2).
Selection of canopy structure by height
above ground
Availability by habitit
The six habitats varied in the availability
of structure at different heights above
Use by macaques and gibbons
Macaques traveled at a median HAG of 23
m in habitat group 1 and 21 m in habitat
group 2. Use by HAG was disproportionate
to availability in habitat group 1
(x2 = 21.18, 8 d.f., p < .01) but not in group
2 (x2 = 9.2, 5 d.f., p > .lo; classes > 28 m
HAG were combined for contingency table
analysis). Macaques favored structure
21-24 m HAG (Fig. 3) both in group 1
(x2 = 16.57, d.f., p < .0001) and in group 2
(x2 = 7.64,l d.f.,p < .01).
Analysis for gibbons was restricted to habitat group 1 because they traveled too infrequently in group 2 habitats. The median
HAG of travel was 31 m. Travel by HAG
classes was disproportionate to the availability of structure (x2 = 20.6, 8 d.f.,
p < .Ol); gibbons preferred to travel in
structure 21-24 m high (x2 = 8.07, 1 d.f.,
p < .01) and 3 7 4 0 m high (x2 = 4.47, 1 d.f.,
p < .05), and avoided structure 13-16 m
high (x2 = 5.19, d.f.,p < .05; Fig. 3).
The gibbons traveled higher than the
macaques in habitat group 1 (median = 31
vs. 23 m; Mann-Whitney test, z = 3.6,
p < .001). The species also varied in their
use of the HAG classes in habitat group 1
(x2 = 20.0, 8 d.f., p < .Ol); gibbons traveled
-0- macaques - habitat group 1
- -&- macaques - habitat group 2
.....- m- gibbons - habitat group 1
Height above ground
Fig. 3. The Jacob's D values calculated for each HAG class. Blackened symbols indicate a significant
result (p < .05)in a 2 x 2 contingency table for that HAG class.
at 3 7 4 0 m HAG (x2 = 4.86, 1 d.f., p < .05)
more frequently than macaques.
1 * macaques
Selection of different-sized trees
Availability by habitat
The habitats did not differ in the availability of trees of various diameters (Kruskal-Wallis test, H = 1.45, d.f., p > .95), so
the data from all six habitats were pooled
into one group. Because neither primate
species traveled in trees < 15 cm dbh, they
were eliminated from the selectivity analysis. Most trees (76%)were 16-31 cm dbh and
few trees were larger than 48 cm dbh.
Use by macaques and gibbons
Considering only trees 2 15 cm dbh,
macaques chose the sizes of trees in which to
travel according to their availability
(x2= 3.91, 3 d.f.,p > .2; Fig. 4). They traveled mostly in trees 16-31 cm dbh (60%)but
showed a slight, nonsignificant preference
for trees 64-122 cm dbh (Fig. 4). Gibbons, in
contrast, were very selective (x2 = 20.11, 3
d.f., p < .0002). Trees of 16-31 cm dbh
(x2 = 4.68, 1 d.f., p < .001) were avoided
while trees of 64-122 cm dbh (x2 = 4.10, 1
d.f.,p < .001) were favored (Fig. 4).
The gibbons traveled in larger trees than
the macaques (median = 48 vs. 26 cm dbh;
Mann-Whitney test, z = 3.5, p < .OOl>. The
distributions of size classes used are also
distinctive (x2 = 11.03, 3 d.f., p < .05) with
Diameter at breast height (cm)
Fig. 4. The Jacob's D values calculated for each DBH
class. Blackened symbols indicate a significant result
03 < .05) in a 2 x 2 contingency table for that DBH
the macaques using the smallest trees,
16-31 cm dbh, more frequently than the gibbons (x2 = 9.6, 1 d.f.,p < .001).
Use of the most continuous stratum
Both species traveled in the most continuous stratum (that with the greatest degree
of horizontal continuity relative to their immediate position; see Methods) almost half
the time (50%for macaques and 46%for gibbons), and yet their distributions differed
(x2 = 13.8, 8 d.f., p < .05 Fig. 5). Gibbons
traveled more often > 15 meters above the
most continuous stratum than macaques
(x2 = 8 . 6 , l d.f.,p < .01; Fig. 5).
Distance from continuous stratum (m)
Fig. 5. The relative percentage of travel by
macaques (n = 69) and gibbons (n = 29) occurring
within different distance classes above (positive values)
or below (negative values) the most continuous stratum.
Comparison of different canopy
use variables
Whitney test, z = 2.37, p < .05), regardless
of whether a female carried an infant, but
the stability and the inclination of these
supports did not differ (Table 1).Supports in
main canopy and emergent trees were more
stable than those in low canopy for both
sexes (x2 = 17.5, 8 d.f., p < .05). Also, in the
main canopy, more negatively inclined supports (-90" to -20") and fewer positively
inclined supports (40"- 60") were used but
in the high canopy, more positively inclined
supports (40"- 60") were used. No sex,
layer, or habitat differences were found in
the median diameter (median = 6 cm), stability (class 1 = did not move) and the angle
(20")of supports used by gibbons. They used
larger diameter supports than the female
macaques while traveling (Mann-Whitney
test, z = 4 . 2 9 , <
~ .001;Table 11, but not significantly larger diameter supports than the
male macaques (Mann-Whitney test, z =
1.43). In the emergent trees, the male
macaque used larger diameter supports
than gibbons (Mann-Whitney test, z = 2.93,
p < .05).
The gibbons traveled higher above ground
within each layer than the macaques
(MANOVA, Fl,2 = 26.9, p < .0001) and
Use of supports while crossing
these layers were used in relation to HAG
between trees
(F1,2= 54.3, p < .0001). The interaction of
species and layer differences in HAG was
Supports were divided between those
also significant (F1,2= 3 . 3 , <
~ .04),but this used on "take-off and "landing" (Table 1)
result is probably a minor interaction be- This division is necessary because the "landtween factors and due to large differences ing" supports were less stable than the takewithin factors (Snedecor and Cochran, off supports for both species (Wilcoxon
1967). The gibbons also traveled higher in signed-rank, macaques, z = 5 . 0 3 , <
~ .0001;
trees matched for the same dbh class gibbons, z = 4 . 4 , <
~ .OOOl). The diameter of
(F1,3= 13.1, p < .0005) and the larger size supports did not differ for either species and
classes used corresponded to greater heights the angle did not differ for macaques. Gibabove ground for both species (Fl,3 = 29.4, bons used supports which were oriented
p < .0001). The interaction between factors more closely to vertical on take-off than
was not significant (F1,B= 0.7 p > 5 ) .The landing (Wilcoxon signed-rank, z = 3.7,
gibbons traveled at greater heights above p < .001).
ground than the macaques while having the
The male macaque launched himself off of
same relationship to the most continuous larger diameter supports than females (Tastratum (Fl,4 = 1 9 . 1 , <
~ .0001), and gibbon ble 1; Mann-Whitney test, z = 2.5, p < .05),
travel which occurred at greater distances and also landed on larger diameter supports
above the most continuous stratum occurred than females (Mann-Whitney test, z = 2.8,
at greater HAGS (Fl,4= 31.9, p < .0001). p < .05). No differences in the stability or
There was a very minor interaction between angle of support were found between sexes,
factors (Fl,4 = 2 . 4 , >
~ .05).
layers, or habitats in either take-offs or
landings. Supports used on take-off for the
Use of supports while traveling
female gibbon carrying a n infant were less
The male macaque traveled on larger di- stable in the high canopy (x2 = 10.6, 4 d.f.,
ameter supports than the females (Mann- p < .05). No other sex differences were
TABLE 1 . Characteristics of supports' used by macaques and gibbons during travel and
while crossinE gavs between trees
Travel supports
Stability3 Angle
Male macaaue
Female macaque
5 (50)
3 (103)
6 (55)
Take-off supports
Landing supports
'Values are median diameter (cm), stability class and angle of inclination of support.
'Numbers in parentheses are sample sizes used in the calculations; n for landing supports is the same for take-off supports
3Stability classes are: 1 = the support did not move, 2 = support slightly moved, and 4 = support moved >.25 but s.5 m.
found in comparisons for the supports used from the understory to the emergent layer.
by gibbons on either take-off or landing, and The mean number of gaps steadily devalues were lumped for the sexes (Table 1). creased (Kruskal-Wallis test, H = 81.6, 4
Gibbons took off from larger diameter d.f., p < .0001; Fig. 6a) from the understory
supports than either the male macaque to the emergent layer. The median width of
(Mann-Whitney test, z = 3.1,p < .01) or fe- gaps initially decreased from the understory
male macaques (z = 5.1, p < .0001). On up to the main canopy but gaps were then
landing, gibbons used larger diameter sup- much wider in the emergent layer
ports than female macaques (z = 4.3, (H = 75.3, 4 d.f., p < .0001; Fig. 6b). The
p < .001). The male and female macaques median length of continuous canopy segused larger diameter and more stable sup- ments generally increased, with a small dip
ports while traveling than while taking off at the high canopy layer (H = 79.0, 4 d.f.,
(diameter: males, z = 2.8; females, z = 3.9, p < .0001; Fig. 6c).
p < .05; stability: z = 5.7, p < .05) or landing (diameter: males, z = 2.5; females, Use by macaques and gibbons
z = 4.5, p < .05; stability: both sexes,
Combining data from all six habitats, a
z = 9 . 1 ,<
~ .05). Gibbons used larger diammajority of gaps present in all layers were
eter and more stable supports while travelwider than 3.5 m, the widest gap crossed by
ing than while taking off (z = 3.7, p < .01;
(Table 2). The narrowest gap
z =5.0,~
< .0001, respectively) and landing macaques
width class (0.1-0.5 m) was the one most
(z = 4.0,~
< .001; z = 9 . 1 , <
~ .0001).
commonly crossed by macaques (50%) but
was rarely available (< 5%)in all layers exSelection of gaps of different sizes for
cept for the main canopy, where such gaps
crossing between tree crowns
comprised 12% of all gaps. The macaques'
Availability by habitat and by layer
use of gap widths strongly favored the narHorizontal continuity in canopy structure rower classes in all layers (Fig. 7) and difamong habitat types was described by three fered from the distribution of gap widths acvariables: (1) the number of gaps encoun- tually available to them. Gibbons crossed
tered in each 20 m sample, (2) the longest gaps up to 9 m wide, so a greater number of
gap encountered in each sample, and (3)the gaps were available t o them than the
longest continuous segment of canopy in macaques. Many gaps were still too wide for
each sample. Measures for each of these them t o cross, particularly in the emergent
three variables did not differ among habi- layer (65%;Table 2). They crossed the sectats for any layer (Kruskal-Wallis test, ond widest gap class (1.6-3.0 m) most comn = 10 for each of six habitats, total number monly (42%).The use of gaps by gibbons difof comparisons = 5 layers x 3 variables fered from the distribution of gap widths
that they could cross (i.e., those G 9 m wide)
= 15; all p's > .05).
To examine differences among canopy lay- only in the main and the high canopy, and
ers, data from all habitats were combined. strongly favored the second class (1.6-3.0 m)
Figure 6 illustrates the strong pattern in the in all layers (Table 2, Fig. 8). Finally, gibcentral tendency of each variable, moving up bons typically crossed much wider gaps than
TABLE 2. Comparisons among canopy layers in crossing
ofpaps b y macwues and gibbons
2.5 1
X2 value
for selectivity of gaps2
macaques gibbons macaques gibbons
% of gaps
too wide to cross1
Main canopy
High canopy
'Based on maximum width of gap observed to be crossed: = 3.5 m for
macaques, 9.0 m for gibbons.
'Selectivity of gaps for crossing (X2 values) are displayed in Figures 7
and 8.
**p< .01, - * p < .001.
layers even though the availability of gap
widths varied (Fig. 6).
Canopy layer
Fig. 6. a: The mean number of gaps between tree
crowns present per 20 m segment (n = 60 at each layer).
Data were combined from all habitats. b: The median
gap width for each canopy layer along the 20 m segment.
c: The median length of the continuous structure segments in each canopy layer. Incomplete segments were
included in all calculations (see Methods).
Specialization of locomotor behavior
Quadrupedal walking was the specialized
mode of locomotion for traveling macaques
(60%) whereas bridging (49%) and leaping
(36%) were the common modes for crossing
between trees (Table 3). Bridging was used
for crossing narrow gaps and leaping for
crossing wide gaps (Table 4); this distinction
is expected because bridging is limited by
body length. In contrast, gibbons most often
brachiated both during travel along supports (48%) and when crossing gaps (57%),
with leaping the next most comrnm mode in
both contexts (Table 3). Bridging rarely occurred (one of 21 occurrences). Leaping is
used for crossing slightly wider gaps than
brachiation (Mann-Whitney test, p < .01,
Table 4). Gibbons would often leap from the
edge of a tree crown across very wide gaps as
the initial mode in the sequence of travel.
Sequencing of locomotor modes
The sequencing of locomotor modes within
each travel segment also varied between the
species (Table 3). Quadrupedal walking and
running appeared more than expected a t the
beginning (x2 = 25.5, 1 d.f., p < .0001) and
at the end (x2 = 26.4, 1 d.f., p < .0001) of
macaque travel segments and less than expected as the second (x2= 21.4, 1 d.f.,
the macaques (median = 2.0 vs. 1.0 m; p < .0001) and the second to last modes
Mann-Whitney test, z = 7 . 2 , ~
< .0001). For (x2 = 40.4, 1 d.f., p < .0001). Leaping, the
both species, the widths of gaps crossed did specialized mode for crossing wide gaps (see
not vary by layer; they use the same widths Table 3), occurred more than expected as the
of gaps in crossing between trees in different second to last mode (x2 = 12.3, 1 d.f.,
low canopy
main canopy
high canopy
Fig. 7. Selectivity of gap widths (Jacob's D values) by macaques within each layer. Gaps > 3.5 m were
included in the calculations but are not depicted because the D value is always -1.0. Significant results
are ( p < .05): in the understory, the low canopy, the high canopy, and the emergent layer, gaps < 1.1 m
were preferred (solid symbols). In the understory and the emergent layer, gaps 1.1-1.5 m were preferred.
Gaps 2.6-3.0 m were avoided in the low canopy.
low canopy
main canopy
high canopy
: : E
Gap width
Fig. 8. Selectivity of gap widths (Jacob's D values) by gibbons within each layer. Gaps > 9.0 m were
included in the calculations but are not represented because the D value is always -1.0. Significant
results are (p < .05):in the main and the high canopy, gaps 1.5-3.0 m were preferred; in the understory
and the emergent layer, gaps 1.1-1.5 m were preferred; gaps &1.5 m were avoided in the main canopy.
p < .001) and less than expected as the last
mode (x2 = 4 . 8 , l d.f.,p < .05). Bridging, the
specialized macaque mode for crossing narrow gaps, appeared more than expected as
the second (x2 = 19.1, 1 d.f.,p < .0001) and
the second to last modes (x2 = 26.9, 1 d.f.,
p < .0001) and less than expected a t the be-
ginning (x2 = 5 . 9 , l d.f.,p < .05)and the end
(x2= 8.4, 1 d.f., p <.01) of travel segments.
In the gibbon travel segments, brachiation
occurred less than expected at the end
(x2 = 9.7, 1 d.f., p < .01; Table 4). Leaping
occurred more than expected at the beginning (x2= 12.4, 1 d.f., p < .0001) and less
TABLE 3. Use of different locomotor modes for travel, for crossing gaps, and during travel sequences
Bipedal walking
Relative %
use while
Relative %
use while
crossing gaps’
Number of observations for each mode
at each step in the travel
to last
‘For macaques, n = 94 and 68 for traveling and crossing gaps, respectively; for gibbons, n = 75 and 21.
*p < .05; * * p < .01; and ***p < .0001: all significance levels are derived from ax2table analysis.
TABLE 4. Median width ofgap crossed by macaques and
aibbons using each locomotorv mode’
Bipedal walking
Number of
gap width (m)
’Tests were Man-Whitney U statistic.
**p < .01, for leaping vs. brachiation in gibbons.
***p < .0001, for bridging vs. leaping in macaques.
than expected a t the end (x2
9.0, 1 d.f.,
p < .01; Table 4).
The organization of travel segments
themselves was clearly limited by tree crossings. Macaques stopped before leaving the
tree in which they began in 26% of all segments, and made only one crossing in 50% of
all segments; the remaining fraction involved two or more crossings. Gibbons were
short segment specialists; 95% of all segments involved no crossings or only one
(47%for each).
The constraint of crossing gaps
The results indicate that crossing the
gaps between tree crowns is a central problem organizing arboreal locomotion by mammals such as gibbons and macaques, which
must cross between hundreds of adjacent
tree crowns, most of which are separated
spatially by significantly wide gaps, to visit
the dispersed patches of fruits and seeds
they prefer to eat. For macaques, in all
strata, the majority of gaps present between
tree crowns are much wider than the gaps
usually crossed (Table 2). For gibbons, a
third of all gaps are too wide (Table 2); the
only circumstance where the widest class of
gaps are not the most common gap widths
present are for gibbons in the main canopy
(Fig. 8). Therefore, although both species
are constrained by gaps from traveling directly between two distant points, macaques
are much more so than gibbons; this distinction supports a central hypotheses for the
evolutionary divergence of apes and monkeys (Temerin and Cant, 1983). The limited
choices for both species explains their repeated travel along “arboreal highways”
through familiar habitat, commented upon
by Ripley (1967) and Whitten (1982), among
Gap crossings influenced several aspects
of macaque locomotor behavior. Their two
specialized modes of locomotion for crossing
these gaps, bridging and leaping, seem inadequate to cross most gaps. Bridging, a very
slow and relatively safe process, is limited
by body length, so it can only occur across
very narrow gaps ( S 1.0 m). Leaping, which
involves higher energy costs and greater
risk, was only used to cross wider gaps.
However, the 3.5 m limit observed in this
study should not be interpreted as a strict
physical limit to macaque abilities; during a
confrontation, the male leapt across a gap of
more than 6 m while chasing a pair of gibbons. The gaps crossed by leaping reflect a
tradeoff between high risk and energy costs
and the benefits from greater directness of
travel. These specialized crossing modes occur as the second and the second to last
modes during travel segments, indicating
that locomotor strategy is organized around
crossing gaps (Table 3) and few travel segments involve more than one crossing. A
segment either begins close to a gap crossing
or stops just after one, as the macaque reconsiders the available options. Leaping occurs towards the ends of segments, probably
because it is not the preferred method for
crossing between crowns and was used only
after the animal has traveled into a situation demanding a leap.
Thinner and hence more flexible supports
are used when macaques cross between
trees, both on take-off and landing (Table 1).
Even though the male used larger supports
than females, because of his greater body
mass, his supports were equally unstable.
Landing supports, although of diameter
equal to take-off supports, were less stable.
Therefore, t o infer the forces involved during travel, the stability of that support is
essential to consider, as well as the size of
support. Because macaques are limited by
the width of gaps in their ability to cross
between crowns, they are forced to cross
from the extreme periphery of crowns in order to minimize the width of crossings. But
this also forces them t o use small supports.
During powerful leaping or precarious
bridging, these are especially flexible, effectively widening the gap and providing an
unstable base for propulsion. Our results
concur with Cant’s (1988), although he observed a higher use of lianas in crossing
gaps, probably because of habitat differences in structure.
Brachiating gibbons, on the other hand,
did not seem t o be as limited in their choice
of travel path nor does their locomotor strategy seem to be as constrained by the problem of crossing between gaps. They did not
exhibit any strong specialization of locomotor mode or sequencing of behavior for crossing gaps (Table 31, but they certainly modified their behavior while crossing gaps.
First, the median gap width (2.5 m) crossed
while brachiating is probably longer than
the “stride length commonly used within a
tree crown (Prueschoft and Demes, 1984).
Second, leaping occurred twice as often during crossings than during travel and was
used to cross wider gaps than was brachiation, although small samples probably prevented statistical significance (Table 3).
Travel supports, both on landing and takeoff, were also smaller and less stable during
crossings than during travel.
A model predicting use of canopy strata
As suggested for macaques, the choice of a
stratum is influenced by three factors: the
availability of gaps which can be easily
crossed, the frequency with which gaps are
encountered per unit distance, and the
length of continuous segments of structure
(Fig. 6 ) .The first variable is determined by a
species’ locomotor morphology and behavior
while the other two depend on canopy structure. To examine whether these three variables can predict strata use by each primate
species, we derived and calculated a Perceived Continuity Index (PCI) for each
strata. The PCI for each species for each
stratrum, i, is defined as:
PCIi = (Ci* Gi/2 * Fi)
in which Ci equals the median length of continuous canopy in the ith layer, Gi equals the
percentage of gaps narrow enough to be
crossed by each species, and Fi equals the
frequency of gaps per 20 meter sample. The
factor 2 in the denominator merely scales
the two species for easy comparison and
does not affect the relative suitabilities of
the strata. A relatively high value of PCI for
a strata indicates it is more continuous from
Fig. 9. The continuity index for each canopy layer for macaques and gibbons, illustrating how each
species can use the different layers as pathways for continuous travel. The index is the product of the
median length of continuous structure by the percentage of gaps between tree crowns which can be
crossed for each layer, divided by the product of two times the mean number of gaps per 20 m sample.
the animal’s perspective and thus is a more
favorable layer for direct, uninterrupted
Figure 9 shows the PCI values for each of
the five measured strata for each primate
species; these relationships are identical to
those for the frequency of use of each layer
(see Fig. 2). This congruence supports the
hypothesis that the nature of the horizontal
continuity within a stratum can predict
which strata will be used by a species, when
modified by its limits to crossing wide gaps.
Further, this match between the use of canopy strata and PCI can be interpreted as
support for the hypothesis (Cant, 1987) that
these two primate species travel in layers
which maximize travel efficiency rather
than because food might be located there.
This PCI model assumes that the immediate goal of locomotion is to move directly
between two points separated by several
tree crowns. In comparing the five canopy
strata in their general suitability for direct
travel, it is clear why the main canopy is
preferred for travel by both species. The
combination of narrow gaps, few gaps per
unit distance and a long median length of
continuous structure, provide the greatest
number of options for direct travel in the
main canopy (Fig. 6). The two primates diverge in their PCIs especially in the upper
strata (Fig. 9). The high canopy and emergent layers are perceived by gibbons as more
continuous. The wider gaps in these layers
(Fig. 6b) are less of an impediment because
gibbons cross wide gaps, so the longer segments of continuous canopy (Fig. 6c) can be
exploited for travel. In contrast, the understory and low canopy combine the unfavorable features of short canopy segments between gaps and wide gaps (Fig. 6).
The application of this model may be limited to arboreal mammals with medium
body sizes feeding on widely dispersed
patches of food such as fruit. If food patches
are sparse, then the cost of moving between
patches is more significant than moving up
or down through the strata after arriving at
a food patch. For small insectivorous primates, travel may typically be combined
with more continuous prey searching, so
that travel layer would likely reflect where
food occurs. For large-bodied males or females carrying infants, and especially for
the very large-bodied orangutan (Cant,
1987, 1992), the actual strength of available
supports may be an important variable in
addition to the nature of gaps. Also, orangutans frequently travel through small trees
by using their large body mass to sway a
small tree back and forth until the tree leans
over enough for them to bridge t o the next
tree (Cant, 1992; pers. obs.). Therefore, although this model predicts the location of
travel by macaques and gibbons quite well,
over a wider range of body sizes and locomo-
tor morphologies and behaviors there may
be other confounding factors that must be
added to the model.
Other factors, such as predation pressure,
may also strongly affect the suitability of a
canopy layer for travel, with the relative
danger of travel in each strata depending on
the type of predator. The congruence between the PCI model and the use of canopy
layers suggests, however, that predators
have only a slight, if any, effect on the canopy layer selected for travel.
would be required to evaluate other plausible factors. Because these factors are likely
to covary, it remains unclear what governs
macaque decision-making about travel
path. Do macaques select the main canopy,
the most continuous stratum, or merely use
the nearest tree which will support them?
Testing ecological and evolutionary
hypotheses of arboreal locomotion
In choosing how and where to travel in the
arboreal environment, primates presumably integrate an enormously complex set of
The explanatory power of canopy
costs and benefits, involving tradeoffs
structural variables
among time efficiency, energy efficiency and
No single variable suffices to describe and risk avoidance (see Cant, 1992). Our samexplain canopy travel by these two primates, ples are too small to allow us to assess how
arguing for detailed investigations. For in- choices of travel path and modes are influstance, within each class of the two struc- enced by the spatial pattern of forest succestural variables, canopy layer and dbh, gib- sional phases and of forest habitats. The six
bons traveled higher than macaques. habitats were delineated by topography and
Further, gibbons traveled higher above the drainage, but differed also in the availabilground than macaques when their relation- ity of canopy layers and structure at various
ship to the most continuous stratum was heights above ground (Fig. 3). The effects of
similar (Fig. 5), indicating that the most these aspects of canopy structure on locomocontinuous stratum was higher above tion have been underemphasized. More deground in tree crowns through which gib- tailed analyses, such as those of Whitten
bons traveled. Because each canopy layer is (1982) and Ganzhorn (19891, if they were to
often several meters thick and the depth of a incorporate the structural variables demonsingle tree crown can be 10 m or more, it is strated to be important in this study, could
probable that gibbons simply travel through link locomotor modes to use of different habthe upper regions of the same type of forest itats, possibly successional stages, and even
as macaques. In sum, a combination of plant species assemblages. Most primate
height descriptors is therefore necessary to home ranges contain several distinct habiexpose subtle differences in travel not cap- tats. If detailed analysis of selectivity, of
structure use versus availability, were made
tured by a single structural variable.
Lack of selectivity among tree sizes for within each habitat, the degree of flexibility
travel (Fig. 4) supports the inference that of locomotor behavior could be evaluated
macaques adopt the simple decision rule of and linked to habitat selection.
choosing the nearest tree crown with the
This study demonstrates that sampling
structural strength and stability to support methodologies can be readily applied to imthem. This makes sense if the height at prove the description of vegetative structure
which macaques travel is driven by the need as it relates to the functional ecology of arboto efficiently cross gaps between tree real locomotion. More detailed measures of
crowns. An animal unable to cross wide habitat structure are an essential next step
gaps, which has to cross numerous crowns in the field study of primate arboreal locoduring its daily ranging, might minimize its motion. Additional variables to be measured
deviation from direct line travel between include the densities of available support
points by choosing the nearest trees which types and the frequency of lianas that cross
offer structural support. Studies of how tree gaps between trees. The variation in the
size (dbh) relates to vertical stratification availability of structure within a forest haband to the interconnectedness of tree crowns itat, among habitats, among maturity
phases, and across an animal's geographic
range, and its behavioral responses, and
that of sympatric species to this variation,
should be essential elements in studies that
explore the fundamental problems of primate ecology, such as habitat selection,
niche relationships and limits to the distributions of species. Much more detailed,
quantitative analysis of the structural environment in which arboreal mammals live is
necessary to separate hypotheses of the
function of postcranial morphology that are
central to the study of primate evolutionary
ecology. We argue that the approach
adopted in this study, in which selectivity
analyses is used to demonstrate preferences
for canopy structures and identify constraints to canopy use, is essential to testing
these ecological and evolutionary hypotheses.
We thank our sponsors, the Center for Research and Development in Biology, of the
Indonesian Institute of Sciences (LIPI), in
particular Dr. Soetikno Wijoatmodjo, Ms.
Moertini Atmowidjojo and Mr. H. Napitupulu, and the Subdirectorate of Nature Conservation (PHPA) of the Ministry of Forestry, in particular Dr. E. Sumardja and Mr.
H. Prayitno, for permission to conduct research in the Gunung Palung National Park
and for logistic support. We thank L. Curran, T. Laman, and P. Palmiotto for assistance at Cabang Panti, and especially D.
Lawrence for support during every phase of
this research. C. Chapman, T. Goldberg, S.
Zens and especially K. Hunt and three anonomous reviewers kindly helped clarify and
refine drafts of this paper. M. Leighton
appreciates grants from the National Science Foundation (BNS-8409299), the Conservation Food & Health Foundation and
the John Merck Fund in support of this
research. The Goelet Fund and the Ford
Foundation Fund for Undergraduate Research, both of Harvard University, the Explorers' Club Youth Activity Fund, and the
Research Experience for Undergraduates
(REU) program of the NSF supported C.
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gibbons, canopy, elements, selection, macaque, gaps, locomotor, crossing, comparative, ecology
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