Locomotor ecology of wild orangutans Pon
SUBJECTS AND METHODS Field study
The field study took place between December 1998 –November 1999 in the Ketambe Research Sta- tion (3°41⬘N, 97°39⬘E) in the Gunung Leuser Eco- system, Northern Sumatra, Indonesia. The area consists mainly of undisturbed primary lowland rainforest (Rijksen, 1978; van Schaik and Mirmanto, 1985). The Ketambe orangutans have been studied almost continuously since the establishment of the research station in 1971, and thus individual ani-
LOCOMOTOR ECOLOGY OF WILD ORANGUTANS
59
mals and their relationships and histories are well- known.
Conditions of visibility ruled out any classification of positional behavior on the basis of footfall pattern or hand/foot grip. Instead, positional classifications are based on the standard categories detailed by Hunt et al. (1996), who categorized both postural and locomotor behavior in terms of the number of weight-bearing limbs and whether each limb ap- pears to be under predominantly suspensory (“ten- sile”) or compressive stress regimes. In this classifi- cation system, the body part that bears the most weight is recorded first in the definition. Body parts which contact a substrate but which do not appear to bear more than their own weights are not included in the locomotor definition (Hunt et al., 1996). Infor- mation on whether the weight-bearing limbs are flexed or extended is also recorded (joints are re- garded as “extended” only when in, or very near, full extension; all other joint positions are recorded as “flexion”).
The first 6 weeks were spent in refining the stan- dard categories given in Hunt et al. (1996) to reflect better the diversity of orangutan locomotion, and in self-training to estimate support and locomotor clas- sifications. Fifty-four biomechanically distinct loco- motor submodes were identified. These will be pub- lished in detail elsewhere, but for the present study they are conflated into seven modes (Table 1). Fur- ther self-training in estimating height and diameter of supports was performed during this time and throughout the data collection period. The main pe- riod of data collection thus took place between Feb- ruary–November 1999.
Apart from the type, number, and diameter of the supports used, the height of the animal in the can- opy, the direction of locomotion, and the contextual behavior, the main group of variables which might a priori be regarded as likely to have influence on orangutan locomotion consists of the age, sex, rank, and body size of the individual. Social rank is less relevant for orangutans than in studies of many other primate species due to their more solitary nature. Further, factors other than age influence the development of secondary sexual characteristics; thus a male orangutan might be adult in years but subadult in development (Utami et al., 1997). There- fore, we define adult males as those exhibiting sec- ondary sexual characteristics such as cheek flanges, throat pouches, and increased body mass, and adult females as females that have given birth. Subadult males are defined as sexually active males that lack secondary sexual characteristics, and immature males and females as subjects that show no sexual activity (Rijksen, 1978). Ten adult and immature individuals from both sexes were observed. See Ta- ble 2 for subject information. It is obviously impos- sible to know the absolute body mass of free-ranging subjects without trapping them, which would have been unethical even were it possible. Subjects were therefore visually ranked according to decreasing body size, particularly when two or more individuals were near one another. These were then classified into the body-size groups specified in Table 2. Vari- ation in body size was substantially greater between groups than within groups, although subadult males were closer in size to adult females than to adult males. Classifications of an orangutan’s age, sex,
TABLE 1. Positional behavior observations
1. Date 2. Individual 3. Time 4. Positional mode 1
Quadrupedal walk: locomotion on top of supports angled at ⬍45°. Typically all four limbs contact support in a particular sequence. Torso is pronograde or roughly parallel to support. Includes tripedal walk, quadrupedal run, and tripedal run. Bipedal walk: hindlimbs provide support and propulsion, with only insignificant contributions from other body parts. Includes flexed and extended bipedalism, and hand-assisted bipedalism in which hindlimbs bear more than 50% of body mass, but one or both forelimbs are used to assist, either in suspension or compression, and bear more than their own weight.
Climb/descent 2 : ascent and descent on supports angled at ⱖ45°. Distinction is made between vertical climb/descent (i.e., climbing on supports within 20° of true vertical) and angled climb/descent (climbing between 20°–45°). Torso-orthograde suspension: includes brachiation and orthograde clamber which is a forelimb suspensory torso-orthograde mode, but with hindlimbs assisting either in suspension or compression. All four limbs act as propulsors, with most of bodyweight borne by abducted forelimbs. Also includes mode drop, in which all predrop postures were orthograde in nature.
Torso-pronograde suspension 3 : all limbs are used in some combination; torso is pronograde, and limbs are in tension. Bridge: a torso pronograde gap closing movement used with limbs both in compression and suspension. Oscillation: combines modes tree sway and ride, although note that “ride” for Sumatran orangutans does not occur from tree to
ground as in Hunt et al. (1996), but from a higher to lower level in canopy. Also includes liana and branch sway, in which body is used to oscillate vertical/subvertical lianas/branches with increasing amplitude to reach next support. These modes are conflated in this study, since all involve significant support deformation.
5. Height: 5 m interval up to 40 m, ⬎ 40m (measured as the vertical distance from the animal to the ground) 6. Number of supports: 1; 2; 3; 4; many 7. Support type: branch, liana, trunk, bough, other (aerial roots, bamboo, nest) 8. Support diameter: ⬍2 cm; ⱖ2–⬍4 cm; ⱖ4–⬍10 cm; ⱖ10–⬍20 cm; ⱖ20–⬍40 cm; ⱖ40–⬍80 cm; ⱖ80 cm (after Cant, 1987) 9. Behavior: feed (acquiring, processing, and eating); travel
10. Clinging infant 1 All follow those of Hunt et al. (1996) unless otherwise stated, and include all submodes as detailed in their study.
2 20° was selected as a convenient midpoint between 0 – 45°. 3 For analysis, pronograde suspension and bridge were conflated, as both had very small frequencies.
60 S.K.S. THORPE AND R.H. CROMPTON
and body size overlap sufficiently for these variables to be combined, to reduce redundancy in the model- ling process, as an age-sex variable, which acts, in this study, in place of a true body mass variable.
Instantaneous sampling on the 1-min mark was used to enable detailed support and behavioral data to be collected, in addition to positional behavior. This method does not take account of the distance travelled during a locomotor bout, but Doran (1992) demonstrated that results obtained with instanta- neous sampling do not differ significantly from loco- motor bout sampling with distance if the sample is large, as is the case in this study. Once located, the orangutans were followed for a maximum of 5 con- secutive days from when they left their night nest (normally around dawn, but in bad weather the time of commencement of travel could approach noon), until they built their next night nest (approximately 5:00 –7:00 PM ). Individuals were followed on at least two well-separated occasions in an attempt to re- duce possible bias associated with temporarily abun- dant fruit.
Table 1 provides details of positional behavior ob- servations for this study. Two variables which might
be expected to have an influence on the relationship between locomotor mode and related ecological vari- ables were omitted from the final analysis. These are the direction of locomotion and substrate angle. While direction of locomotion was recorded and ini- tially included in our statistical model, it was re- moved at an early stage, as its measurement in the field is problematic (dramatically increasing the number of cells with zero or small frequencies), and it is not independent of locomotor mode definitions (e.g., vertical climbing). Support angle was also re- corded, but the results are not presented because of the need to reduce the number of variables and categories.
One female (Ans) travelled with a dependent in- fant. During observation it was noted whether the infant was clinging or travelling independently, as Sugardjito and van Hooff (1986) found slight differ- ences in locomotor repertoire before and after par- turition. However, Ans’ locomotion did not differ significantly when the infant was clinging compared to when it was travelling independently.
Statistical analysis
The interdependence of observations is a further problem in the analysis of locomotor data. Sequen- tial observations using a small time interval are thought to produce results in which assumptions of independence may be violated, so that sampling pro- cedures may be required (Boinski, 1989; Hunt, 1991; Dagosto, 1994; Warren and Crompton, 1997). How- ever, due to poor visibility in this study and the tendency of orangutans to rest frequently during bouts of locomotion, sequential observations were rarely obtained. Consequently, we feel that the de- pendence between data points is of minimal concern here, and all locomotor observations are analyzed. To eliminate interobserver variation, one of us (S.K.S.T.) obtained all 28,797 instantaneous obser- vations of positional behavior, 2,811 of which were of locomotion, the subject of the present report. It should be noted that 47% of observed locomotor bouts sampled behavior of immature males and fe- males, 35% that of adult females and 19% that of adult and subadult males, so that there is a degree of undersampling of the behavior of the latter. How- ever, since body weight was only one of a number of variables included in the log-linear analysis, it would be inappropriate to weight the data on this basis.
Like any form of multivariate analysis, log-linear analysis should be regarded as first and foremost a means of exploring the data. Thus, we need to go into the process of analysis (or modelling) in some detail. We indicated above that our concern is to explore the relationship between the potential loco- motor repertoire of orangutans (what they can do) and the habitat in which they live: the expression of this relationship is locomotor behavior. This behav- ior can be thought of as a data-space influenced by a number of different variables, which may also have influence on each other. In hierarchical log-linear modelling, we ask which combination of interacting variables exerts a statistically significant influence on the data-space, and which best “explains” this data-space while leaving as little as possible (the residual) unexplained (for a detailed treatment, see Agresti, 1990).
TABLE 2. Study subjects 1
Age-sex category Name
No. focal
days
Notes Adult 么
Bobby
10 Dominant male AM2
5 Unidentified young adult male Adult 乆
Yet
3 c. 34
14 Dominant female, travels with immature son Yossa (see below) Sina
3 c. 29
11 Mid-rank, pregnant, travels with immature son
Ans
3 24 11 Low rank, travels with semi-dependent infant
2 21 3 Eldest offspring of Yet Immature 乆
Chris 4 12 12 Independent daughter of Ans Immature 么
Eibert 4 8 13 Independent Yossa
4 7 13 Son of Yet 1 ⫺, unknown.
LOCOMOTOR ECOLOGY OF WILD ORANGUTANS
61
Log-linear analysis works, like the familiar 2 test, by comparing actual cell counts in a contin- gency table to theoretically expected values (in this case, values predicted by the models). Like the chi- square test, it is thus most effective when there are as few variables as possible and as few empty or near-empty cells as possible. Iteratively, the proce- dure seeks the smallest “model,” i.e., variable-com- bination, which creates predicted cell-counts best fitting the observed cell counts in the multiway con- tingency tables. A significance value of 1 for the 2 likelihood ratio indicates a perfect fit of the model’s predicted cell counts to the observed cell counts. In the first instance, terms (variable-interactions) with
a significance value less than 0.05 are iteratively deleted. (Note that a large value for P in log-linear analysis thus has an almost “opposite” implication, e.g., to the value of P in a t-test.) Generally, one cannot expect to find one single best-fit model or “variable-combination” which explains all relation- ships between variables. As is typical of multivari- ate statistics, the analyst exercises informed judg- ment progressively to identify those variables and variable-combinations which best explain the field observations, aided in this case by biological inter- pretation of the adjusted residuals in the multiway contingency tables. These indicate by their sign whether a particular interaction is more (⫹ve) or less (⫺ve) common than predicted by the model, and by their size, to what degree (for details, see Agresti, 1990).
Once a best-fit model or models are established on the basis of the parameter P (the significance level of the 2 likelihood ratio), the relative importance of interactions included within a model is indicated by
the rank of the standardized 2 values ( 2 /DF, e.g.,
last column in Table 8). For the best-fit models, we then proceed to determine the strength of relation- ships between variables from standardized cell re- siduals (SCRs) in the multiway contingency tables (e.g., Table 9) and calculate the odds ratios. These represent ratios of probabilities and enable the cor- relations underlying the significant interactions to
be identified (Crook, 1997). For example, for the interaction age-sex * behavior * height in Figure 1, of the 752 observations of adult females travelling in the study, 603 travelled below 20 m. The probability that a female will travel below 20 m is therefore 603/752 (0.80), and the probability that females will move above 20 m is 149/752 (0.20). The odds ratios of these probabilities, i.e., 0.80/0.20, is 4, which estab- lishes a correlation between females and height in the canopy, with an adult female being four times more likely to travel below 20 m than above. The legitimacy and statistical reliability of this type of multidimensional statement, which we might previ- ously have had to make at considerable risk of mis- interpretation by analyzing a series of combinations of two-dimensional tables, lie at the heart of the power of the log-linear approach to analyze interac- tions between habitat and locomotor behavior.
Our analysis was performed using SPSS version
10.07 (Chicago, IL).
Sections of the analysis
Support type and diameter were only recorded for bouts in which between 1– 4 supports (e.g., up to one per limb) were used, as, in practice, it was impossi- ble to record such fine details when more than four supports were used during an observation. Conse- quently, the data are analyzed in two parts. Ini- tially, the relationships between locomotion and age-sex category, number of supports, height, and contextual behavior are analyzed for all observa- tions (n ⫽ 2,811, the “basic” analysis). Then a more detailed analysis is presented for the observations which include data on support type and diameter (n ⫽ 1,648, the “support” analyses), again in respect to their relationship with locomotion.
Conflation, recategorization, and selection of variables
As with two-way contingency table analysis, the power of log-linear analysis is undermined if more than 20% of cells within a multiway contingency table have an expected frequency of less than 5 (Tabachnick and Fidell, 1996), and it is therefore often necessary to collapse, or conflate, variables with more than two categories. However, suitable category combinations are not always immediately apparent. For locomotion, modes which are biome- chanically distinct are not necessarily also statisti- cally distinct when viewed in relation to support and behavioral-ecology variables, and the choice of cate- gories for the other variables is necessarily rather arbitrary (e.g., should height be separated into 10-, 15-, or 20-m intervals?). We therefore created new substitute variables (see the Tables 3 and 4 for clas- sifications) which classify categories in alternative ways, selecting the substitute variables on the basis of the strength of their relationship to other vari- ables (as indicated by analysis of the adjusted resid-
Fig. 1. Basic model interaction: age-sex * behavior * height. Values in boxes are standardized cell residuals.
62 S.K.S. THORPE AND R.H. CROMPTON
LOCOMOTOR ECOLOGY OF WILD ORANGUTANS
TABLE 3. Substitute classifications tested in log-linear analysis
Original variable
Substitute classification
male; female
Age-sex-1 Age-sex-2 Age-sex-3
2. No. of supports
No. of supports-1 No. of supports-2 No. of supports-3
3. Height
Height-1 Height-2 Height-3
4. Behavior
Behav
travel; feeding
5. Support type
Type-1
branch, bough, trunk, other Type-2 liana, other, tree
6. Support diameter
cm
TABLE 4. Substitute locomotor classifications tested in log-linear analysis
Locomotor classification
Categories
LOCO-A, all separate 1) quadrupedal, 2) oscillation, 3) bipedal, 4) pronograde suspend, 5) orthograde suspend, 6) climb/descent
pronograde suspend, 5) climb/descent
climb/descent combined climb/descent, 4) pronograde suspend, 5) vertical climb/descent orthograde suspend, 5) climb/descent suspend, 5) orthograde suspend
descent combined combined, bipedal separate
orthograde suspend, 5) climb/descent descent, 4) orthograde suspend orthograde suspend, 4) climb/descent
combined bipedal combined
orthograde suspend, 4) climb/descent
ride LOCO-L, suspension, compression, mix
uals). Height, for example, was reclassified in three females and immature subjects as separate catego- ries, and No.supports-3, which distinguishes simply between the use of single and multiple supports.
In the “support” studies, analysis of all variables together (age-sex category, locomotor mode, height, last proved the most effective in explaining the re- behavior, number of supports, support type, and lationships between our variables by leading to bet- support diameter) was impossible, as there were ter-fitting models, both in the basic and support more possible combinations between variables than analyses. In each case, better-fitting models also observations. Analyses of associations between more included the substitute variable age-sex-2, which than four variables resulted in very high levels of combines adult and subadult males, leaving adult sampling zeros. Consequently the models of best fit
64 S.K.S. THORPE AND R.H. CROMPTON TABLE 5. The three best-fitting models for basic analysis 1
Substituted locomotion
Partial classification
2 DF 1 Significance level (P)
Model expressions (variable relationships) LOCO-D
age-sex * locomotion * height * no. of supports age-sex * locomotion * no. of supports * behavior locomotion * height * behavior age-sex * height * behavior height * no. of supports * behavior
LOCO-E 14.724
age-sex * locomotion * height * no. of supports age-sex * locomotion * no. of supports * behavior locomotion * height * behavior age-sex * height * behavior height * no. of supports * behavior
LOCO-F 15.448
age-sex * locomotion * height * no. of supports age-sex * locomotion * no. of supports * behavior age-sex * height * behavior locomotion * height * behavior height * no. of supports * behavior
1 DF, degrees of freedom.
were found for variable subsets which looked at the cluded in the models of statistical best fit (Table 6) relationship between locomotor mode, number of differed between the variable analysis subsets A, B, supports, support type, support diameter, and: A, and C. Consequently, to identify which substitute age-sex; B, height; and C, behavior.
locomotor variable and which substitute diameter We further minimized the number of variable variable best represented the whole support analy- combinations by combining data concerning support sis dataset (i.e., all data in subsets A, B, and C type and number of supports used, e.g., the substi- together), we calculated the mean values of signifi- tute variable Type-2 has categories liana and other; cance (P), degrees of freedom, and sampling zeros for tree; multiple liana and other; multiple tree; mixed each substitute locomotion and diameter classifica- liana, other and tree (Table 3). Similarly, support diameter and number of supports were combined, an overall statistic for each combination (Table 7).
Log-linear analysis requires judgment to be exer- cised between retention of detail in categories and relationships, and goodness of fit: in some cases, for example, a better result in terms of desirable fea-
observations in which 2, 3, and 4 supports are used, tures (a high significance level, P, but a low percent- age of sampling zeros, and simple interactions) was the best associations with other variables in the achievable by excluding rare data, such as observa- “basic” analysis.
tions on supports of over 10 cm in diameter (35 It was also found necessary to conflate bipedalism, cases). Similarly, use of the substitute variable Lo- quadrupedalism, and pronograde suspension with co-C, while not in the top three models of fit in the other modes of locomotion, because these modes con- basic analysis, gave a better balance than those that sistently resulted in large adjusted residuals. Differ- were (Loco-D, -E, and -F, Table 5) in terms of a ent combinations were again essayed for each, based relatively high P while minimizing complex interac- on analysis of the relevant adjusted residuals (Lo- tions, and while performing better than Loco-H, -I, co-B to Loco-I for bipedalism, and Loco-D and Lo- and -J in terms of retained detail. Loco-C was also co-G to Loco-I for the latter two; Table 4).
the most frequently occurring substitute locomotor
variable in the 10 overall statistically best-fitting models in the Table 7 for support analyses. Thus
Model selection
The three statistically best-fitting models in the Loco-C was selected as the substitute locomotor basic analysis (see Table 5) included substitute lo- variable which provided the best description of loco- comotor variables Loco-D, Loco-E, and Loco-F, but motion, in relation to the other tested variables. they were in other respects less desirable, in that they retained complex, second-order (four-way) vari- able interactions, while Loco-C, -H, -I, and -J re- tions. solved one of these into two simpler, first-order
Table 8 gives the models (sets of associations) for (three-way) variable interactions. In the support the chosen substitute locomotor and diameter vari- analyses, substitute variables which retained de- ables, for the basic analysis and support analysis tailed distinctions between locomotor modes gener- subsets A, B, and C. The sets of associations re- ally led to better-fitting models than those which mained the same when the minimum P for retention conflated locomotion into only a few categories. But of terms (variable-associations) was raised from 0.05 the substitute locomotor and diameter variables in- to 0.07, indicating a robust fit. The best-fit models
65
LOCOMOTOR ECOLOGY OF WILD ORANGUTANS
TABLE 6. The three best-fitting models for support analyses 1 Substituted
Substituted diameter
locomotor
Partial 2 1 Significance
Model expressions Subset A (age-sex)
DF level (P)
type * diameter age-sex * diameter locomotion * diameter age-sex * locomotion age-sex * type locomotion * type
type * diameter age-sex * diameter locomotion * diameter age-sex * locomotion age-sex * type locomotion * type
type * diameter age-sex * diameter locomotion * diameter age-sex * locomotion age-sex * type locomotion * type
Subset B (height)
LOCO-J
15.22 28 0.976
locomotion * height * type locomotion * height * diameter type * diameter
LOCO-C
22.73 35 0.946
locomotion * height * type type * diameter locomotion * diameter height * diameter
LOCO-C
34.59 48 0.927
locomotion * height * type type * diameter locomotion * diameter height * diameter
Subset C (behavior)
LOCO-C
61.32 74 0.854
locomotion * behavior * type type * diameter locomotion * diameter
LOCO-C
62.25 75 0.854
locomotion * behavior * diameter type * diameter locomotion * type behavior * type
LOCO-B
47.54 57 0.810
locomotion * behavior * diameter type * diameter locomotion * type behavior * type
1 DF, degrees of freedom.
TABLE 7. The ten overall best-fitting models for support analysis 1
Model Diameter classification
Degrees of Sampling rank
Locomotor classification
Significance level
freedom zeros (%)
for the support analyses cannot be regarded as a full are first tested for no association between variables description of the associations between variables, (main effects) and then all two-way associations, all since each analysis excludes two variables. To test three-way interactions, and so forth. The results for whether the exclusions falsely increased clarity, all our chosen substitute variables Loco-C and Diam 2 variables were analyzed together, using a SPSS log-
: 1,420.52, 2 linear forward selection approach in which the data
implies that when all variables are modelled, the relationships between the variables are described sufficiently by all two-way associations. While these results are not reliable in terms of model selection (as the high significance levels for all two-way and all three-way models are a reflection of the large number of sampling zeros rather than an accurate representation of the fit of the model), they do imply that the addition of the support data, to some extent, resolves the complex (i.e., three- and four-way) vari- able interactions in the basic model, into a series of simpler two-way associations between variables.
RESULTS Descriptive data
Descriptive statistics are not the focus of this pa- per, and will be described in detail elsewhere. How- ever, to summarize the main results, orangutan lo- comotion is dominated by orthograde suspension, which accounts for 48% of the total locomotor reper- toire. Orangutans are 2.4 times more likely to ex- hibit orthograde suspension than vertical climb/de- scent, nearly 3 times more likely to exhibit orthograde suspension than quadrupedalism, and over 7 times more likely to do so than to exhibit pronograde suspension and oscillation. With regard to the age-sex category, 47% of observed locomotor bouts sampled behavior of immature individuals, 35% adult females, and 19% adult and subadult males. Sixty-six percent of locomotion took place below 20 m, and orangutans spent 27% of locomotor bouts feeding and 71% travelling. Finally, 59% of observed bouts utilized more than one support for weight-bearing.
Influences on locomotion
The variable relationships in the larger dataset (i.e., the basic analysis; Table 8) indicate that loco- motion is influenced by height, behavior, number of supports, and age-sex category. The magnitude of the association between locomotion and height dif- fers according to whether orangutans are travelling or feeding (behavior * height * locomotion, Table 8). The number of supports used for different locomotor modes differs when moving above or below 20 m (height * no. of supports * locomotion, Table 8). The existence of a second-order interaction (age-sex * behavior * no. of supports * locomotion, Table 8) shows that the number of supports used for each locomotor mode in travel and feeding differs accord- ing to the age-sex category of the individual. Overall height and behavior are conditionally dependent, given age-sex (age-sex * behavior * height, Table 8), locomotion (behavior * height * locomotion, Table 8), or number of supports (behavior * height * no. of supports, Table 8). Only the variable age-sex is not in a three-way interaction with locomotion. This suggests that when the associations between all variables are taken into account, the age-sex cate- gory of the individual has limited influence on the observed locomotor repertoire. The magnitude of the
2 values associated with the interac- tions of the different variables (Table 8) shows that
the combined influence of height and behavior ac- counts for more of the variation in locomotion than the combined influence of height and number of supports, and has over three times more influence than the interaction between age-sex category, no. of supports, and behavior. However the interaction “age-sex * height * behavior” is over twice as impor- tant as the most important expression for locomo-
TABLE 8. Models of best fit and associated standardized 2 values 1
Model
Model expressions
2 Degrees of freedom
2 /degrees of freedom) Basic
age-sex * behavior * height 36.094 2 18.05 behavior * height * locomotion
28.654 4 7.16 behavior * height * no. of supports
5.882 1 5.88 height * no. of supports * locomotion
19.980 4 5.00 age-sex * behavior * no. of supports * locomotion
16.125 8 2.02 Support Subset A (age-sex)
type * diameter 2,191.255 16 136.95 locomotion * diameter
197.168 16 12.32 locomotion * type
137.998 16 8.62 age-sex * diameter
42.659 8 5.33 age-sex * type
27.049 8 3.38 age-sex * locomotion
19.929 8 2.49 Subset B (height)
type * diameter 2,166.127 16 135.38 height * diameter
43.552 4 10.89 locomotion * diameter
171.623 16 10.73 height * locomotion * type
46.461 16 2.90 Subset C (behavior)
type * diameter 2,188.352 16 136.77 locomotion * type
144.823 16 9.05 behavior * type
15.282 4 3.82 behavior * locomotion * diameter
34.479 16 2.15 1 2 values correspond to most important interactions and are ranked for each model accordingly.
66 S.K.S. THORPE AND R.H. CROMPTON
LOCOMOTOR ECOLOGY OF WILD ORANGUTANS
TABLE 9. Contingency table for support model association: type * diameter 1 Support diameter
Multiple ⬍10 Total Liana
Support type
5.2* Multiple lianas
13.4* Multiple trees
28.9 19.3 12.7 9.6 29.6 100.0 1 Entries are row % and (column %) for each type * diameter unit, e.g., for locomotion on lianas with diameters of ⬍10 cm, 71.9% of all locomotion on lianas was on ⬍10-cm diameters, and 25.3% of all locomotion on diameters of ⬍10 cm was on lianas. Asterisks denote
standardized cell residuals (negative values indicate frequency is lower than expected). ⫺, structural zeros which are omitted from modeling procedure and do not affect accuracy of model.
tion. The second-order interaction “age-sex * behav- of a single tree support occurs almost 5 times as ior * no. of supports * locomotion” has a very low often as the use of a single liana, over 6 times as standardized chi-squared value, indicating that the often as the use of multiple lianas, and over 12 times magnitude of the relationships between these vari- as often as the use of mixed tree and liana supports. ables is rather weak.
Overall, the most utilized diameter category was Interaction effects (Table 8) for the smaller data- “multiple ⬍10 cm,” with an odds ratio of 3.1 over the set, the support analysis, show that all tested vari- least used category, “mixed,” indicating that oran- ables do influence locomotion in some form. Al- gutans are over 3 times more likely to utilize multi- though “support type * diameter” is the only ple supports under 10 cm than multiple supports of association common to all models, we can see that different diameters. The study subjects tended to locomotion has a two-way (direct) association with use “⬍10 cm” and “multiple ⬍10 cm” in a similar age-sex category, support type, and support diame- proportion, but when using one support, orangutans ter (subset A, “age-sex”). However, the relationship are 1.5 and 2.3 times, respectively, more likely to use between locomotion and support type differs when “⬍10 cm” than “10 –20 cm” and “⬎20 cm.” Overall, moving above and below 20 m (subset B, “height”). nearly 60% of locomotion relied exclusively on sup- Similarly, the association between locomotion and ports of ⬍10 cm in diameter (Table 9, column total support diameter when travelling differs from that for “⬍10 cm” and “multiple ⬍10 cm”).
when feeding (subset C, “behavior”). Comparison of 2 Analysis of contingency tables
the standardized values associated with variable interactions (Table 8, subsets A–C) shows that the
We see in Table 8 that support diameter is the association “support-type * diameter” is over 11 most important influence on observed locomotor rep- times stronger than the next expression. When age- ertoire, when support characteristics are included in sex (subset A) and height (subset B) are included in the analysis. Table 10 gives details on this relation- the analysis, support diameter appears to be the ship, and to highlight our interpretative technique, most important influence on locomotion. It is five we discuss this contingency table in detail, together times more important than age-sex category, and with related material on support type and locomo- slightly more important than support type in subset tion in Table 11, and on the three-way interaction
A, and over 4 times more important than the com- between behavior, locomotion, and support diameter bined influence of type * height in subset B. In (Table 12). An identical interpretation of Tables contrast, when contextual behavior is considered 13–15 and Figures 1–5, which present the relation- (subset C), support type is over 4 times more impor- ship between the age-sex category and associated tant than the combined influence of diameter * be- variables, is the source of other similar relationships havior. This may be related to the fact that the highlighted in the Discussion. subset C (“behavior”) data were found to be better
described when diameter was reclassified to recog- Locomotion * diameter nize a 4-cm demarcation.
Orthograde suspension is by far the most prevalent
Support type and diameter
form of locomotion for all diameter categories except “⬎20 cm,” where levels are substantially reduced and
Seventy-eight percent of all locomotion takes quadrupedalism is twice as likely to be exhibited (Ta- place only on trees (branches, boughs, and trunks), ble 10, column percentages). Orthograde suspension is with 51% on single tree supports and 27% on mul- particularly associated with single supports of ⬍10 cm tiple tree supports (Table 9). Odds ratios calculated diameter, and is between 4 – 8 times more likely to be from the same contingency table show that the use exhibited than comparable locomotor modes (“quadru-
68 S.K.S. THORPE AND R.H. CROMPTON TABLE 10. Contingency table for support model association: locomotion * diameter 1 Support diameter
Multiple ⬍10 Total Quadrupedalism
3.9* Orthograde suspend
1.3* Pronograde suspend
⫺0.1* Vertical climb/descent
28.9 19.3 12.7 9.6 29.6 100.0 1 For explanation of table, see Table 9.
TABLE 11. Contingency table for support model association: locomotion * type 1 Support type
Multiple trees Total Quadrupedalism
Multiple lianas
3.7* Orthograde suspend
⫺1.5* Pronograde suspend
0.1* Vertical climb/descent
10.0 49.5 4.0 8.0 28.4 100.0 1 For explanation of table, see Table 9.
TABLE 12. Contingency table for support model interaction: behavior * locomotion * diameter 1 Support diameter
Multiple ⬍10 Total Travel
Behavior Locomotion
3.1* Orthograde suspend
1.1* Pronograde suspend
0.2* Vertical climb/descent
2.6* Orthograde suspend
0.6* Pronograde suspend
⫺0.6* Vertical climb/descent
25.7 21.7 13.4 12.1 27.1 100.0 1 Entries are row % and (column %) for behavior * locomotion * diameter unit, e.g., for quadrupedalism on ⬍10 cm in travel: 16.2%
of all quadrupedalism was on ⬍10 cm diameters, and 10% of all locomotion on ⬍10 cm diameters was quadrupedalism. Asterisks denote standardized cell residuals (negative-values indicate frequency is lower than expected).
pedalism,” “pronograde suspend,” and “oscillation”) on multiple), occurring infrequently or not at all on the multiple supports ⬍10 cm in diameter (“multiple other diameter categories. ⬍10,” Table 10). “Oscillation” also shows strong asso-
We can further see that “quadrupedalism” is ciations with supports of ⬍10 cm (both single and strongly associated with larger, single supports (a
LOCOMOTOR ECOLOGY OF WILD ORANGUTANS
TABLE 13. Contingency table for basic model interaction: behavior * height * locomotion 1 Height
20 m Total Travel
Orthograde suspend
Pronograde suspend
Vertical climb/descent
Orthograde suspend
Pronograde suspend
Vertical climb/descent
48.5 51.5 100.0 1 For explanation of table, see Table 12.
Total
TABLE 14. Contingency table for support model interaction: height * locomotion * type 1 Support type
Height Locomotion
Multiple trees Total 20 m
Multiple lianas
3.2* Orthograde suspend
1.5* Pronograde suspend
1.5* Vertical climb/descent
2.0* Orthograde suspend
0.4* Pronograde suspend
1.5* Vertical climb/descent
5.5 60.2 1.6 2.5 30.3 100.0 1 For explanation of table, see Table 12.
total of 56% occurring on diameters “10 –20 cm” When climbing or descending vertically, orangutans common than expected (Table 10, negative values and “multiple 10-cm” diameter supports relatively
for standardized cell residuals (SCRs)) on single equally, with these diameter categories being 1.6,
1.9, and 2.2 times more likely to be associated with
4.2 and 2.8 times more likely to be exhibited on a diameters, respectively (Table 10, row percentages). However, vertical climbing represents a larger pro-
spectively. portion of the total locomotor repertoire on mixed Since “vertical climb/descent” can only occur in a supports than on other support diameters, account- vertical plane, its relative frequency is of course not ing for 31% of locomotion on mixed supports (Table directly comparable to the other locomotor modes.
10, column percentages).
70 S.K.S. THORPE AND R.H. CROMPTON
TABLE 15. Contingency table for support model 1 single trees than other forms of locomotion (Table
association: height * diameter Support
Locomotion * diameter * behavior
The association between locomotion and diameter
(Table 10) changes somewhat when the behavioral
context of the observed bout is also taken into ac-
count (Table 12). Orthograde suspension is more
associated with travel than with feeding, but the
pattern of support diameter use for “orthograde sus-
pend” does not differ substantially between behavior
categories (Table 12, row percentages). For both
Total
“travel” and “feeding” there is a strong association
1 For explanation of table, see Table 9.
cm in diameter (as indicated by the large, positive SCRs in Table 12). In contrast, there is a poor asso- ciation between orthograde locomotion and supports
negative SCRs), where there is a preference for qua- drupedalism in both behavior categories (as indi- cated by the large, positive SCRs in Table 12).
“Oscillation” is also more associated with travel cm,” where oscillation is 11 times more likely to be
exhibited in travel rather than feeding (column per- cm combined” relative to levels for the other diame- height categories.
The association between “quadrupedalism” and
Fig. 2. Support model association: age-sex * locomotion. Val-
larger single supports is apparent in both behavior
ues in boxes are standardized cell residuals. Q, quadrupedalism; OS, oscillation; OR, orthograde suspension; PR, pronograde sus- pension; VC, vertical climb/descent.
Similarly, the lower than expected frequency for
Locomotion * support type
Orthograde locomotion is the predominant mode is exhibited in approximately the same proportions for moving on all support types except single lianas, in both “travel” and “feeding.” However, for “10 –20 which shows a stronger relationship with vertical climb (odds ratio for vertical climb * liana / ortho- cm” and “mixed” supports, it has a more dominant
role in “feeding” than in “travel,” being 1.8 and 2.6 times (respectively) more likely to be exhibited.
centages). The strongest correlation between “ortho- Pronograde suspension is exhibited at near pre- grade suspend” and support type is for multiple dicted frequency on all support diameters during
“travel,” but shows a stronger association with loco- and 40.5 times more likely to exhibit “orthograde motion on single supports of 10 –20 cm during “feed-
suspend” than “quadrupedal,” “oscillation,” and ing” (SCRs). When feeding, orangutans ascend and “pronograde suspend,” respectively. Pronograde sus- pension is distributed rather evenly among support
10-cm” supports, but frequencies for travelling are types, except for “multiple lianas,” for which the less than predicted (SCRs). The frequency for climb-
proportion of “pronograde suspend” is rather low ing on single supports of “10 –20 cm” during feeding (negative SCR value).
When vertical climbing, orangutans are 1.6 and higher than expected frequency of vertical climbing
4.1 times more likely to use a single tree support than a single liana or multiple lianas, respectively, 0.8), and in comparison to the average probability of and are 8.9 times more likely to use a single tree vertical climbing in feeding. support than “mixed” support types (Table 11, row percentages). However, orangutans show a stronger
DISCUSSION
affinity for vertical climbing on single lianas than The way in which variables are categorized for and exhibit comparatively less vertical climbing on statistical analysis directly influences the nature of
LOCOMOTOR ECOLOGY OF WILD ORANGUTANS
Fig. 3. Basic model interaction: age-sex * behavior * locomotion * no. of supports. Values in boxes are standardized cell residuals. Q, quadrupedalism; OS, oscillation; OR, orthograde suspension; PR, pronograde suspension; VC, vertical climb/descent.
Fig. 4. Support model association: age-sex * diameter. Values Fig. 5. Support model association: age-sex * type. Values in in boxes are standardized cell residuals.
boxes are standardized cell residuals.
data trends, with some interesting results. Log-lin- relationships found between variables. As a conse- ear models which combine subadult males with quence of the detail in which field data were col- adult males consistently result in better-fitting mod- lected in this study, we were able to experiment with els than those which combine subadult males with variable classifications ranging in complexity, and adult females, or separate them into an individual identify those which exposed the main multivariate category to highlight size-related trends. This sug- data trends, with some interesting results. Log-lin- relationships found between variables. As a conse- ear models which combine subadult males with quence of the detail in which field data were col- adult males consistently result in better-fitting mod- lected in this study, we were able to experiment with els than those which combine subadult males with variable classifications ranging in complexity, and adult females, or separate them into an individual identify those which exposed the main multivariate category to highlight size-related trends. This sug-
Our results (“basic analysis”) also show that the number of supports used is best understood when multiple supports are combined into a single cate- gory. This suggests that while orangutans adopt a different approach to locomotion on multiple sup- ports from that used for one support, it does not change whether they are moving on two reasonably large supports or handfuls of foliage. This result further highlights the importance of analyzing all supports used, rather than focusing on the main weight-bearing support (as did Cant, 1987a) when addressing differences in support use of large-bodied arboreal animals: fully 59% of orangutan locomotion involves the use of more than one support.
We noted above that the three models of best fit for subset A (“age-sex”) and subset B (“height”) and the five overall models of best fit for the support analysis (Table 8) incorporate support diameters de- fined in 10 cm intervals, whereas the three models of best fit for subset C (“behavior”) incorporate the 4 cm demarcation. This implies that smaller supports are more critical to observed differences in behavior than they are to differences in the height of observed locomotion or to the differences in locomotor reper- toires of different age-sex categories.
Locomotion
Orthograde suspension dominates orangutan lo- comotion, as Cant (1987a) showed. It is used to resolve habitat problems associated with moving on both single and multiple small supports (⬍10 cm) (Table 10), and plays a slightly larger role in travel than in feeding (Tables 12 and 13). It is used in a comparable way above and below 20 m, except that the standardized cell residuals indicate that it plays
a particular role in traversing multiple lianas below
20 m (Table 14). Oscillatory locomotion is essentially a travel mode which is strongly associated with single and multi- ple supports of ⬍10 cm in diameter (Table 10). How- ever, since it is reliant on support compliance, it is by definition restricted to these smaller-diameter supports. Orangutans oscillate both trees and lianas during locomotion. Tree and branch sway were pre- viously documented by Mackinnon (1974), Sugard- jito (1982), Sugardjito and van Hooff (1986), and Cant (1987a,b, 1994). However, only Mackinnon (1974) previously recorded (although not quantified) liana sway, which is a “Tarzan”-type movement in which the orangutan swings horizontally on one or more vertical lianas with increasing amplitude to reach the next support. Orangutans tend to favor multiple tree supports for oscillatory locomotion both above and below 20 m, although above 20 m there is also a strong association with multiple li- anas (Table 14, column percentages). The use of
multiple supports enables them to distribute their weight onto a number of different supports to max- imize the magnitude of oscillation. This preference is likely to be influenced by support distribution. Below 20 m there are a multitude of young trees, which may be oscillated about the trunk, whereas, above 20 m, the number of compliant trunks is con- siderably reduced, and orangutans must oscillate parts of trees (boughs or branches) or vertical lianas.
Levels of oscillation in travel are comparable to those observed by Cant (1987a) and by Sugardjito and van Hooff (1986), except that the latter authors found levels of oscillation for adult males to be over twice as high as in the present study. In our study, adult males tended to remain comparatively high in the canopy (Fig. 1), and since oscillation is predom- inantly associated with travel below 20 m (Table 13), our results show relatively low frequencies of oscil- lation in adult and subadult males. This contrast should be interpreted with some caution, however, as there are differences in methodology. Further- more, the results of Sugardjito and van Hooff (1986) referred to the locomotor behavior of a single adult male, whereas our data combine 3 subadult males and 2 adults. These show substantial difference be- tween individuals, with oscillation accounting for 16% of Bobby’s locomotor repertoire, 10% of the un- identified adult male’s (AM2’s), and an average of only 5.5% for the subadult males, which is less than that of adult females and immature individuals. It is therefore likely that the single adult male of Sug- ardjito and van Hooff (1986) exhibited a particular preference for this mode of locomotion.
Quadrupedalism is strongly associated with sta- ble single supports of ⬎10 cm in diameter, occurring notably less than expected for single and multiple supports of ⬍10 cm (Table 10). Its strong association with tree supports (Table 11) is presumably because of the lack of horizontally oriented lianas, and be- cause tree supports reach much larger diameters, which is clearly preferable for quadrupedal locomo- tion (indeed, this is one reason why captive orangu- tans appear more quadrupedal, as cage furniture is often rigid, e.g., as in Crompton et al., 2003). It is exhibited more in feeding than in travel (Table 12), and is performed twice as often above 20 m as below (Table 14). In the “basic model,” quadrupedalism is more associated with movement above 20 m than any other locomotor mode, for both travel and feed- ing, with the association being particularly strong for feeding above 20 m (Table 13).
The locomotor classification “pronograde suspend” is a rather arbitrary conflation of pronograde sus- pension and bridging locomotion, formed to reduce the number of small and zero cell frequencies in the contingency table. However, in the modelling pro- cess, analysis of adjusted residuals did not indicate problems with this classification. This implies that, despite positional differences, pronograde suspen- sion and bridging behavior do not differ in their relationship with other variables in the study.
72 S.K.S. THORPE AND R.H. CROMPTON