Brief Report Received: May 21, 2001 Accepted: July 5, 2001

Folia Primatol 2001;72:292–297

Congruence of Tail Use Behaviors between Male and Female Mantled Howling Monkeys (Alouatta palliata) Brandon Wheeler a Peter Ungar b a Interdepartmental

Doctoral Program in Anthropological Sciences, Department of Anthropology, SUNY Stony Brook, N.Y., and b Department of Anthropology, University of Arkansas, Fayetteville, Ariz., USA

Key Words Primates W Positional behavior W Locomotor behaviors

Introduction

Differences between males and females in locomotor and positional behaviors have been documented for several primate species [1, 2]. In Alouatta palliata for example, females climb and use smaller substrates more than males [3–5]. Such sex differences are usually related to body size. Indeed, interspecific studies have repeatedly demonstrated relationships between body size and locomotor and positional behaviors. It is easier, for example, for a large primate to suspend beneath a branch than to balance on top of it [6, 7]. This is particularly true for primates that feed near the periphery of the crown, where branches tend to be smaller. Allometric effects on tail use between species have also been noted, such that larger prehensile-tailed primate taxa use their tails more than do smaller ones [8]. The prehensile tail in relatively large howlers, for example, is generally viewed as an adaptation to facilitate suspension during terminal branch feeding [3, 8–11]. One might further expect that larger males would use their tails more for support and weight-bearing than would females. To date, however, little attention has been paid to sex differences in prehensile tail use. Tail use is compared between male and female mantled howlers (A. palliata) in the contexts of different activities and while on different substrates. We test the hypothesis that, because male mantled howlers are about 30% heavier than females [12], they will

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Peter Ungar, Department of Anthropology Old Main 330, University of Arkansas Fayetteville, AR 72701 (USA) Tel. +1 501 575 6361, Fax +1 501 575 6595 E-Mail [email protected]

Table 1. Data collected during this study (modified from Bergeson [8], Bezanson, unpubl. data)

Category

Options

Description

Degree of tail use

None Wrap Weight Only

Tail wrapped around support, but no weight borne Some weight borne by tail and some by other limb(s) All weight borne/animal suspended by tail

Support size

Small Medium Large

Support can be encircled by one hand (of focal animal) Support can be encircled by both hands Support too large to be encircled by both hands

Support angle

Horizontal Oblique Vertical

! 15° 15–75° 1 75°

Activity

Rest Feed Travel

use their tails more for support and weight-bearing. Results indicate no significant differences in tail use between the sexes. This is interpreted within the context of significant differences in tail use related to differing activities and substrate types.

Methods Data were collected during more than 300 h of observation from May through July, 1999, at the La Suerte Research Station. The study area is an advanced secondary forest in northeastern Costa Rica [13]. The group studied was well habituated, and included 10 individuals (3 adult males, 5 adult females and 2 juveniles). Data on degree of tail use, general activity, substrate size, and substrate orientation (table 1) were collected for all adults in the group. These data were recorded at 2-min intervals using instantaneous focal animal sampling [14]. Focal animals were selected at the beginning of each day to maximize data for each individual. Individuals were followed until tree cover obscured behaviors. Subsequent focal animals were chosen as the first adult to come into view on a new support. Differences between males and females in tail use were assessed relative to general activity type, substrate size, and substrate orientation. Data were analyzed using two-factor multivariate analyses of variance (MANOVAs) following procedures described by Ungar [15]. Percentages of observations in which a given tail use type occurred for each sex during different activities and on substrates of differing sizes and orientations were tallied for 5-day intervals. Five-day intervals were chosen to maximize representation of tail use behaviors in each category, to minimize chances of non-independence of replicates, and to assure sufficient replication for statistical analysis. Data for activity type, substrate size and substrate orientation were analyzed separately with sex as the other independent variable, tail use types as dependent variables, and rank-transformed [16] sums of percentages of observations over each 5-day interval as the replicates. Separate ANOVAs and subsequent Bonferroni pairwise comparisons on the ranked data were used to assess sources of significant variations. These tests determined (1) whether males and females differed in the ways they used their tails, (2) whether howlers differed in tail use while engaged in different activities and on different sorts of substrates, and (3) whether there were any sex differences in tail use when controlling for activity or substrate type (i.e., whether there was an interaction between these variables).

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Table 2. Statistical analyses

MANOVA models: Wilk’s Ï and degrees of freedom

A

Overall Sex Variable 2 Interaction

Size

Angle

Behavior

0.004* (4.45) 0.922 (4.45) 0.337* (8.90) 0.751 (8.90)

0.009* (4.45) 0.963 (4.45) 0.321* (8.90) 0.843 (8.90)

0.014* (4.45) 0.947 (4.45) 0.070* (8.90) 0.918 (8.90)

* p ! 0.001. ANOVA models: F values and degrees of freedom for individual tests

B

Behavior Only Weight Wrap None

32.212* (2.48) 25.527* (2.48) 29.821* (2.48) 139.881* (2.48)

Size 35.673* (2.48) 11.211* (2.48) 0.350 (2.48) 7.122* (2.48)

Angle 0.816 (2.48) 0.457 (2.48) 12.505* (2.48) 0.340 (2.48)

* p ^ 0.002. Bonferroni models: Pairwise mean differences

C

Size large ! medium Only Weight None

2.611 3.361 –0.278

large ! small 23.556* 17.972* –14.556*

medium ! small 20.944* 14.611* –14.278*

Angle horizontal ! oblique Wrap

–4.278

horizontal ! vertical –20.389*

oblique ! vertical –16.111*

Behavior feed ! rest Only Weight Wrap None

–23.806* –23.444* –3.222 18.722*

feed ! travel –18.944* –20.889* –25.944* 35.111*

* p ! 0.015.

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Wheeler/Ungar

rest ! travel 4.861 2.556 –22.722* 16.389*

Fig. 1. Percentages of summed focal observations in each tail use category by sex for behavioral activity (a), substrate size (b), and substrate angle (c).

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Results

Results are presented in figure 1 and table 2. First, all three tests showed significant variation. Second, none of the three tests evinced a significant sex effect or interaction between sex and the other variable. Third, tests on activity type, substrate size, and substrate angle all showed significant variation independent of sex (p ! 0.001). In other words, these data show no evidence that male and female mantled howlers differ in tail use behaviors, either overall or when considered relative to specific activities, substrate sizes, or substrate orientations. On the other hand, individuals of both sexes did use their tails differently when they were moving, resting or feeding and when they were on branches of differing sizes and orientations. Results indicate that howlers (1) bore weight or suspended by the tail more when on smaller branches, (2) wrapped their tails for support less while on vertical than oblique or horizontal branches, and (3) bore weight or suspended by the tail more when feeding, and wrapped their tails for support less while traveling than during other activities.

Discussion

We predicted that male and female mantled howlers would differ in degrees and incidences of tail use, because larger primate species with prehensile tails tend to use those tails more than smaller species, and that male howlers are significantly larger than females. Results presented here are not consistent with this hypothesis. In fact, males and females did not differ in tail use patterns regardless of activity or substrate type examined. One might argue that the lack of differences between the sexes may actually reflect limitations of data collection or analysis. A type II error is unlikely, however, because differences in tail use for different activity and substrate types (independent of sex) were shown to be significant at p ! 0.001. These results are also surprising given demonstrated differences between male and female howlers in other aspects of locomotor and positional behaviors [3–5]. It seems in this case, however, that tail use behaviors in A. palliata are species-specific, and relate to the activities individuals are engaged in and the substrates they are using [8] rather than to differences between males and females.

Acknowledgments We are grateful to the Molina family, especially Federico Molina for permission to collect data at La Suerte. We also thank Thad Bartlett, Michelle Bezanson, Kimberly Dingess, Francois Larose, Jennifer Weghorst and Eric Worch for helpful discussions related to this project. This study was funded by a grant from the State of Arkansas Information Liaison Office.

References 1 2

296

Cant JGH: Effects of sexual dimorphism in body size on feeding postural behavior of Sumatran orangutans (Pongo pygmaeus). Am J Phys Anthropol 1987;74:143–148. Doran DM: Sex differences in adult chimpanzee positional behavior: The influence of body size on locomotion and posture. Am J Phys Anthropol 1993;91:99–115.

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Wheeler/Ungar

3 4 5 6 7 8 9 10 11 12 13 14 15 16

Mendel F: Postural and locomotor behavior of Alouatta palliata on various substrates. Folia Primatol 1976;26: 36–53. Burns C: An investigation of the functional significance of sexual dimorphism to intraspecific variation in feeding patterns of howler monkeys. Am J Phys Anthropol 1979;50:423. Gebo DL: Locomotor and postural behavior in Alouatta palliata and Cebus capucinus. Am J Phys Anthropol 1992;26:277–290. Grand TI: A mechanical interpretation of terminal branch feeding. J Mammal 1972;53:198–201. Cartmill M, Milton K: The lorisiform wrist joint and the evolution of ‘brachiating’ adaptations in the Hominoidea. Am J Phys Anthropol 1977;47:249–272. Bergeson DJ: The Positional Behavior and Prehensile Tail Use of Alouatta palliata, Ateles geoffroyi, and Cebus capucinus; PhD thesis, Washington University, St Louis 1996. Cant JGH: Locomotion and feeding postures of spider and howling monkeys: Field study and evolutionary interpretation. Folia Primatol (Basel) 1986;46:1–14. Tomblin DC, Cranford JA: Ecological niche differences between Alouatta palliata and Cebus capucinus comparing feeding modes, branch use, and diet. Primates 1994;35:265–274. Bergeson DJ: Patterns of suspensory feeding in Alouatta palliata, Ateles geoffroyi, and Cebus capucinus; in Strasser E (ed): Primate Locomotion. New York, Plenum, 1998, pp 45–60. Fleagle JG: Primate Adaptations and Evolution. New York, Academic Press, 1999. Garber PA, Rehg JA: The ecological role of the prehensile tail in white-faced capuchins (Cebus capucinus). Am J Phys Anthropol 1999;110:325–339. Altmann J: Observational study of behavior: Sampling methods. Behavior 1974;49:227–267. Ungar PS: Patterns of ingestive behavior and anterior tooth use differences in sympatric anthropoid primates. Am J Phys Anthropol 1994;95:197–219. Conover WJ, Iman RL: Rank transformations as a bridge between parametric and nonparametric statistics. Am Stat 1981;35:124–129.

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