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Orangutans Employ Unique Strategies to Control Branch Flexibility

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Orangutans Employ Unique Strategies to Control Branch Flexibility Orangutans employ unique strategies to control branch flexibility Susannah K. S. Thorpea,1, Roger Holderb, and Robin H. Cromptonc aSchool of Biosciences and bDepartment of Primary Care and General Practise, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom; and cDepartment of Human Anatomy and Cell Biology, University of Liverpool, P.O. Box 147, Liverpool L69 3GE, United Kingdom Edited by C. Owen Lovejoy, Kent State University, Kent, OH, and approved June 17, 2009 (received for review November 17, 2008) Orangutans are the largest habitually arboreal mammal. For them, Thus, orangutans may be unusual in an ability to benefit from as for all arboreal mammals, access to the abundant fruits and branch compliance, by using elastic energy stored in compliant narrowest gaps found among the thin peripheral branches of tree branches during tree sway (a locomotor mode where they crowns poses considerable safety risks and energetic demands. oscillate vertical, compliant tree trunks with increasing magni- Most arboreal primates use flexed-limb postures to minimize tude to cross gaps). Tree sway crosses given gaps for less than half problems caused by branch compliance and instability. Here, we of the cost of jumping and an order of magnitude less than the show that Sumatran orangutans employ unique locomotor strat- cost of crossing terrestrially (8). Our recent studies also have egies to control compliance and allow access to the terminal branch demonstrated the surprising result that orangutans frequently niche for feeding and gap crossing. We calculated a ‘‘stiffness use hand-assisted bipedal locomotion to access the fine terminal score,’’ which is a measure of the flexibility of the supports on branches of trees (9), just where the greatest problems with which orangutans moved. We found that certain locomotor be- compliance are likely to occur. This allows orangutans to max- haviors clearly are associated with the most compliant supports; imize stability by using their long prehensile toes to grip multiple these behaviors appear to lack regular limb sequences, which small branches and a hand to further aid balance, while freeing serves to avoid the risk of resonance in branch sway caused by the remaining hand to reach out for feeding or weight transfer. high-frequency, patterned gait. Balance and increased stability are Because the Sumatran orangutan (Pongo abelii) is the largest achieved through long contact times between multiple limbs and habitually arboreal primate (10) and has one of the broadest supports and a combination of pronograde (horizontal) and or- repertoires of positional behavior of all of the primates [con- thograde (vertical) body postures, used both above branches and sisting of Ͼ100 biomechanically distinct postural and locomotor in suspension underneath them. Overall, adult females seem to be behaviors (11)], we hypothesize that this repertoire includes the most conservative in their travel, selecting more solid and unique locomotor strategies for dealing with the flexibility of secure supports than males and adolescents. These results have supports during arboreal travel. However, we expect that thresh- implications for understanding locomotor diversity in fossil and olds must exist below which supports become too compliant for extant apes and for orangutan conservation and reintroduction safe locomotion. Our hypothesis further predicts that orangutans programs. will use locomotion and support combinations close to these thresholds to minimize both the length of travel paths between biomechanics ͉ hominoid evolution ͉ locomotor ecology ͉ food sites and the energetic cost of travel. Because falls from positional behavior ͉ compliance great heights are of greater risk for large animals, we further expect that adult males will choose to travel on more stable supports than adult females and adolescents. In testing these n recent years, researchers have discovered a great deal about hypotheses, this article expands on our previous specific studies Ithe way in which animals move during steady locomotion on (8, 9) to explore the dynamic between compliant arboreal flat terrain, but remarkably little is known about how animals supports and the full range of orangutan locomotion. move in complexly structured environments (see, e.g., ref. 1). The most structurally complex, and speciose, land environment Results and Discussion may be the canopy of tropical rainforest, which presents a During a year-long field study of wild Sumatran orangutans, we three-dimensional meshwork containing unpredictable changes obtained 2,811 instantaneous visual observations of orangutan in the continuity and nature of the supports available for locomotion from 10 individuals and of the supports on which locomotion. In this habitat, arboreal animals, such as primates, they moved (see Materials and Methods). To assess the effect of must cope with one problem in particular that rarely exists for support compliance on locomotion in a diverse locomotor terrestrial animals: the flexibility (compliance) of the supports habitat, we calculated a ‘‘stiffness score’’ (SS), which is essen- against which they must exert forces to support or propel tially a measure of the mean support diameter used for each bout themselves. in which up to four supports were used (see Materials and Flexible branches effectively add another spring in series with Methods). A small SS indicates that the supports are more the animal’s locomotor system and therefore will significantly compliant, and a large score indicates that they are more rigid. disturb normal movement dynamics. Compliant supports have We used a general linear model (GLM) with ln(SS) (the natural been shown to increase the energetic cost of locomotion in log of the stiffness score) as the response variable to adjust for monkeys and lemurs (2, 3) and the cost of takeoff in birds (4). the range of physical, ecological, and behavioral factors that may They further may affect energetics by forcing arboreal animals influence orangutan locomotion (12), including the number, to adopt longer travel routes to circumvent gaps in the canopy. types, and angles of supports used, contextual behavior, height There are also significant, size-related safety implications; falls in the canopy, direction of travel, body size, and individual, here from great heights likely will be fatal to large animals (5, 6), and even falls between levels of the canopy may result in serious injury. The risk of these will be greater on the fine, terminal Author contributions: S.K.S.T. designed research; S.K.S.T. performed research; S.K.S.T. and branches of trees (the terminal branch niche), where resources R.H. analyzed data; and S.K.S.T. and R.H.C. wrote the paper. such as fruits and the narrowest gaps between tree crowns most The authors declare no conflict of interest. often are found, because the vibrations caused by the body mass This article is a PNAS Direct Submission. of even small animals will be much greater (7). 1To whom correspondence should be addressed. E-mail: [email protected]. 12646–12651 ͉ PNAS ͉ August 4, 2009 ͉ vol. 106 ͉ no. 31 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0811537106 Downloaded by guest on October 1, 2021 Table 1. General linear model for dependent variable: Natural logarithm of stiffness score Source Type III sum of squares Degrees of freedom Mean square F Significance Corrected model 454.080* 40 11.352 34.105 0.000 Intercept 275.975 1 275.975 829.116 0.000 Locomotion 48.330 9 5.370 16.133 0.000 Support type 113.230 7 16.176 48.597 0.000 Support angle 8.470 9 0.941 2.827 0.003 No. of supports 8.313 1 8.313 24.975 0.000 Age–sex 15.103 2 7.552 22.687 0.000 Height 26.885 4 6.721 20.193 0.000 Locomotion ϫ no. of supports 10.220 8 1.278 3.838 0.000 Error 492.293 1,479 0.333 Total 8,434.962 1,520 Corrected total 946.373 1,519 *R2 ϭ 0.480 (adjusted R2 ϭ 0.466). represented by a summary age–sex variable (see ref. 12 and Nevertheless, although orthograde behaviors account for the Materials and Methods). The effect of each variable on ln(SS) was greatest proportion of locomotion on supports with smaller tested, and to explore further the relationship between ln(SS) stiffness scores in this study (Fig. 1), pronograde (horizontal and locomotion, we also tested the effect of two-way interactions trunk) bridging allows movement on the smallest mean support between locomotion and all other variables on ln(SS). The final sizes and has a significantly smaller mean SS than orthograde model shows that locomotion, the number, type, and angle of suspension and bipedalism. Sway (which incorporates postures supports used, height in the canopy, age–sex category, and the of all descriptions) also allows locomotion on smaller supports interaction term (locomotion ϫ number of supports) combine than orthograde behaviors, but this result is not statistically significantly to explain ln(SS) (Table 1). Tukey’s difference significant, because sway forms part of subset 2 as well as subset between means tests were performed on the GLM interaction 1 in Fig. 1. Together, these results indicate that locomotor ANTHROPOLOGY term and main effects to identify significant patterns in the versatility is a crucial component of the ability of orangutans to dataset (Figs. 1–5). navigate small supports. The great apes (including humans) are generally thought Although pronograde bridging accounts for only 0.7% of the (reviewed in, e.g., ref. 13) to share morphological adaptations in orangutan’s locomotor repertoire, the musculoskeletal system of the upper limb and trunk for orthograde (vertical trunk) posture animals must adapt to the most strenuous activities in which they and locomotion [but not necessarily suspension (14)], reflecting are used (19) as well as to the most frequent. Pronograde the demands of ripe-fruit-eating in the peripheral canopy of trees bridging places orangutan anatomy under very different stresses in tropical forests (15, 16).
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