Primates (2015) 56:183–192 DOI 10.1007/s10329-015-0457-3
ORIGINAL ARTICLE
Ontogeny of positional behavior and support use among Colobus angolensis palliatus of the Diani Forest, Kenya Noah Thomas Dunham
Received: 18 September 2014 / Accepted: 18 January 2015 / Published online: 4 February 2015 Ó Japan Monkey Centre and Springer Japan 2015
Abstract In this project I studied black and white colobus monkeys (Colobus angolensis palliatus) inhabiting the Diani Forest of south coastal Kenya to test whether activity budgets, positional behavior, and support use differed among individuals in three age categories (juveniles, subadults, and adults). Data for three habituated groups were collected from June to August 2012 and from May to July 2014. Instantaneous sampling and pooled data were used to create overall behavior profiles for the three age categories. Activity budgets differed significantly among the categories. Adults rested more and moved less, subadults socialized more, and juveniles moved more often than individuals in the other two age categories. Support use differed, with juveniles and subadults accessing smaller supports more frequently (i.e., juveniles: bough 19.4 %, branch 57.9 %, twig 13.5 %; subadult: bough 18.6 %, branch 64.5 %, twig 8.2 %) whereas adults preferred larger supports (i.e., adults: bough 32.1 %, branch 54.0 %, twig 5.3 %). Despite different support use, locomotor profiles were remarkably consistent among age categories (i.e., ranges: quadrupedal walk 35.0–45.2 %, bound 17.5–25.3 %, climb 11.2–22.7 %, leap 15.1–19.9 %). Sitting was the predominant posture, accounting for 89.5–92.5 % of the posture observed for all age categories. Overall positional profiles of adults and subadults were statistically indistinguishable whereas juveniles differed significantly from adults but not from subadults. It is hypothesized that the different frequency of specific locomotor behaviors, for example bounding, is attributable to
N. T. Dunham (&) Smith Laboratory, Department of Anthropology, The Ohio State University, Room 4005, 174 W 18th Ave, Columbus, OH 43210, USA e-mail:
[email protected]
morphological changes associated with ontogeny. Nonetheless, these findings support the notion that primates achieve adult-like positional behavior competence during the juvenile life stage. Keywords Primate locomotion Posture Black and white colobus
Introduction Musculoskeletal anatomy affects how primates move through and orient themselves within their environments. Several early studies attempted to link skeletal morphology with specific positional behaviors or a range of behaviors (Erikson 1963; Ashton and Oxnard 1964; Prost 1965; Napier 1967; Stern and Oxnard 1973). Subsequent studies revealed that predictions of behavior based solely on morphological features were not always corroborated by field observations (Ripley 1967; Mittermeier and Fleagle 1976). Because relationships between behavior and morphology among extant primates are used to infer the behavior of fossil forms (Kay 1984; Nakatsukasa et al. 2007), it is imperative to understand the extent of intraspecific positional behavior variation associated with a specific anatomy. Although variation of positional behavior in relation to forest structure and other ecological conditions has been examined in several studies (Garber and Pruetz 1995; Gebo and Chapman 1995a; McGraw 1996; Dagosto and Yamashita 1998; Manduell et al. 2012; Dunham and McGraw, 2014), much less is known about the extent to which changes associated with ontogenetic musculoskeletal development affect positional behavior. This is significant, given that research has revealed that aspects of primate
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limb anatomy (i.e., limb length, muscle development, joint geometry, center of mass) do not scale isometrically and presumably constrain positional behavior in different ways throughout an individual’s development (Hurov 1991; Wells and Turnquist 2001; Young 2005, 2012; Lawler 2006). For example, Young (2005) found that both forearm extensor and forearm flexor muscles scaled to body mass with positive allometry, but that mechanical advantage scaled to body size with negative allometry for two species of capuchin monkeys (Cebus albifrons and Cebus apella). It is hypothesized that the greater mechanical advantage characteristic of infants and juveniles may provide unique selective advantages, for example facilitating more efficient suspensory locomotion and enhancing stability while clinging to the abdomen of another individual (Young 2005). Given these different scaling relationships, it is reasonable to predict significant intraspecific differences in positional behavior among different age classes of a particular species. Nevertheless, despite the different frequency of some individual behaviors, field and laboratory studies have shown that overall positional repertoire is usually conserved intraspecifically across ages (Doran 1992, 1997; Inouye 1994; Thorpe and Crompton 2005; Workman and Covert 2005; Bezanson 2006, 2009, 2012; Lawler 2006; Prates and Bicca-Marques 2008); however, some studies have reported significantly different positional behavior throughout ontogeny (Doran 1997; Wells and Turnquist 2001; Bezanson 2006, 2009, 2012). Given that previous studies have not yielded consistent results, investigation of the extent to which ontogeny affects intraspecific variation in positional behavior continues. I examined this issue by studying the positional repertoire of Peters’ Angola black and white colobus monkeys (Colobus angolensis palliatus) inhabiting the Diani Forest of south coastal Kenya, testing the null hypotheses of no significant differences among: (1) activity budgets; (2) locomotor behavior; (3) postural behavior; and (4) support use for three age classes.
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description of the forest structure composition is provided by Dunham and McGraw (2014). The climate is characterized by two rainy seasons, with short rains from October– December and long rains generally occurring from March– June (Mwamachi et al. 1995). Annual rainfall averages 744 mm (Mwamachi et al. 1995), and temperature ranges from 35 °C in dry seasons to 28 °C in rainy seasons (Okanga et al. 2006). Six primate taxa inhabit the Diani Forest: the small-eared galago (Otolemur garnettii), the Kenya coast galago (Galagoides cocos), vervet monkeys (Cercopithecus aethiops), Sykes’ monkeys (Cercopithecus albogularis), yellow baboons (Papio cynocephalus), and C. a. palliatus. Study species Colobus angolensis palliatus (Fig. 1) are found in a variety of forest habitats throughout Tanzania and southeastern Kenya. Forest destruction is the largest threat to this taxon (Rodgers 1981; Anderson et al. 2007; Preston 2011), the IUCN status of which is currently under review with the recommendation the status be amended from ‘‘least concern’’ to ‘‘threatened’’ (Cunneyworth 2013). The few studies conducted on C. a. palliatus suggest they are similar to other Colobus spp. with a predominantly folivorous diet, small group sizes (the mean group size at Diani is six individuals), and an energy-conservation lifestyle (Lowe and Sturrock 1998; O’Dwyer 2011; Wijtten et al. 2012; Dunham and McGraw 2014).
Methods used to study behavior Positional behavior and support-use data were collected from June to August 2012 and from May to July 2014 for three habituated groups ranging in size from 5 to 12
Methods Study site Kenya’s Diani Forest is part of the Zanzibar–Inhambane floristic region and is one of the few remaining patches of biodiversity-rich coral rag forests in East Africa (Metcalfe et al. 2009). The forest is located in the Kwale District of south coastal Kenya (4°150 3000 , 4°350 3000 S and 39°350 0000 , 39°340 3000 E), measures approximately 455 ha in area (Anderson et al. 2007), and comprises a gradient of intact forest interspersed with degraded areas. A more detailed
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Fig. 1 Subadult female Angola black and white colobus monkey (Colobus angolensis palliatus) feeding from a seated position in the Diani Forest, Kenya
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individuals. Because no significant differences were observed between 2012 and 2014 data, the data for each group were combined. Behavior data were collected from dawn (6:00) until dusk (18:00) for three age classes: adult (*6–10 kg), subadult (*3.5–5.5 kg), and juvenile (*1.5–3 kg). Body mass was based on data from rehabilitation of C. a. palliatus cared for by Colobus Conservation and from naturally deceased specimens collected from the Diani Forest (Cunneyworth, unpublished data). Because no significant differences were observed between the behavior of the sexes, data were combined to create overall activity, locomotor, posture, and support use profiles for each age category. Individuals were distinguished on the basis of combination of body size, facial features, and tail morphology and coloration. I used an instantaneous time point sampling scheme in which data were collected for a single individual every 3 min. Individuals were sampled on a rotational basis, and, to maintain data independence, no individual was sampled twice within 15 min (McGraw 1996). At each time point I recorded: (1) activity: feed, forage (i.e., feeding while moving) move, rest, social, and other; (2) positional behavior (Table 1); and (3) support type (Table 1). A total of 9,020 time-point samples were collected during 642 hours of observation. Statistics G-tests of interdependence (Sokal and Rohlf 1981) were used to compare overall activity, locomotor, posture, and support-use profiles (Doran 1992, 1993; McGraw 1996, 1998a, b; Dunham and McGraw 2014). Because G-tests can only be used to determine whether overall profiles differ, Z-tests were used to compare proportions of individual behavior (Gerstman 2008). Statistical tests were performed by use of SAS 9.3 statistical software.
Results Activity budgets Activity budgets for the three age categories are shown in Table 2. Individuals in all age categories followed the same trend: resting [ feeding [ moving [ socializing [ foraging. Overall comparisons of activity budget profiles revealed significant differences among the age categories (Table 3). Comparisons of individual activity categories also yielded several significant differences (Table 4). Adults rested significantly more (64.3 %) than subadults (51.2 %) and juveniles (52.2 %). Subadults and juveniles spent significantly more time feeding (29.8 % and 29.1 %, respectively) than did adults (24.7 %). Time spent moving significantly decreased from juveniles (12.7 %) to subadults (8.3 %) and
185 Table 1 Positional behavior and support types Locomotor behaviora Quadrupedal walk: relatively slow, pronograde quadrupedal locomotion Quadrupedal run: faster version of quadrupedal walk, includes diagonal sequence gaits and galloping Bound: quadrupedal pronograde locomotion in which the both hindlimbs contact simultaneously followed by both forelimbs contacting simultaneously Leap: locomotion with aerial phase between discontinuous supports characterized primarily by hindlimb extension with landing including hindlimbs and/or forelimbs Climb: vertical or near vertical (support angle [45°) ascent in which forelimbs reach above head and hind limbs push the animal up Arm swing: locomotion involving forelimb suspension (e.g., brachiation, bimanualism) Postural behaviora Sit: ischia bear most of body weight with torso relatively orthograde Stand: all four limbs extended on a relatively horizontal support with torso pronograde Supported stand: standing posture in which at least two limbs are extended on a relatively horizontal support with one or more limbs flexed or reaching out; torso may be orthograde or pronograde Prone lie: lying posture with most of body weight on the ventral surface; limbs may be dangling below support or tucked under body Recline: lying posture with most of body weight on dorsum or lateral aspect of torso Forelimb suspension: below-support hanging posture using one or more appendages Cling: flexed limb posture on relatively vertical support Support typesb Bough: large supports, [10 cm in diameter, so large that adult monkeys cannot fully grasp with hands or feet Branch: medium-size supports, between 2 and 10 cm in diameter and small enough for adult monkeys to grasp with hand and feet Twig: small supports, \2 cm in diameter, usually found on the terminal end of branches Vertical trunk: vertical support of any diameter to which the monkey must cling a
Categories follow Hunt et al. (1996)
b
Categories follow Mittermeier (1978)
to adults (5.7 %). Subadults spent significantly more time socializing (7.6 %) than did adults (3.3 %) and juveniles (2.9 %). Finally, adults foraged significantly less (1.5 %) than subadults (2.5 %) and juveniles (2.9 %). Locomotor behavior Quadrupedal walking was the most common mode of locomotion among all age categories. Frequencies of
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Table 2 Activity budgets, positional behavior, and support use for the three age classes of C. a. palliatus
Table 3 Comparison of overall activity budgets, positional behavior, and support use for the three age classes of C. a. palliatus
Age class
Activity budget
Overall comparison using G-test
Adult
Subadult
Juvenile
(n = 5548)
(n = 1335)
(n = 2137)
Feed
24.7
29.8
29.1
Forage Move
1.4 5.7
2.5 8.3
2.9 12.7
Rest
64.3
51.2
52.2
Social
3.3
7.6
2.9
Other
0.6
0.4
0.2
(n = 383)
(n = 139)
(n = 326)
Quad. walk
45.2
42.4
35.0
Bound
25.3
23.0
17.5
Climb
11.2
18.0
22.7
Leap
16.2
15.1
19.9
Other
2.1
1.4
4.9
Locomotor behavior
Postural behavior
(n = 5,156)
(n = 1,186)
(n = 1,807)
Sit
89.5
91.1
92.5
Prone lie
5.7
5.4
4.0
Recline
3.9
2.7
1.6
Stand Other
0.8 0.1
0.5 0.3
1.1 0.8
(n = 5,548)
(n = 1,335)
(n = 2,137)
32.1
18.6
19.4
Support use Bough Branch
54.0
64.5
57.9
Twig
4.3
8.2
13.5
Other
5.3
6.0
6.3
bounding, climbing, and leaping were lower and more varied (Table 2). Pairwise comparisons of overall locomotor profiles revealed significant differences between adult and juvenile locomotor profiles (Table 3). All other pairwise comparisons of overall locomotor profiles revealed no significant differences. Comparisons of individual locomotor behavior revealed marked differences between adults and juveniles, whereas the locomotor behavior of subadults were generally bracketed by those of adults and juveniles (Table 4). For example, juveniles walked quadrupedally and bounded significantly less often (35.0; 17.5 %) than did adults (45.2; 25.3 %) but climbed substantially more (22.7 %) than did adults (11.2 %). Frequencies of leaping did not differ significantly among juveniles (19.9 %), subadults (15.1 %), or adults (16.2 %).
Adult vs. subadult
Subadult vs. juvenile
Adult vs. juvenile
Activity budget
G = 101.8, P \ 0.01
G = 52.4, P \ 0.01
G = 156.6, P \ 0.01
Locomotion
ns
ns
G = 24.9, P \ 0.01
Posture
ns
G = 9.8, P = 0.02
G = 35.0, P \ 0.01
Support use
G = 133.0, P \ 0.01
G = 27.8, P \ 0.01
G = 288.3, P \ 0.01
posture profiles for juveniles differed significantly from those for adults and subadults (Table 3). Comparison of individual postural behavior (Table 4) revealed that juveniles lay prone significantly less (4.0 %) than adults (5.7 %) and subadults (5.4 %). All pairwise comparisons of recline were significant and frequencies of this posture increased from juveniles (1.6 %), to subadults (2.7 %), to adults (3.9 %). Standing comprised a small percentage of the postural behavior of all age categories (0.5–1.1 %). Support use Support-use data for each age category are reported in Table 2. For all age categories, branches were the most commonly used type of support, followed by boughs and twigs. Use of vertical trunks, artificial supports, and the ground all constituted small percentages of overall posture profiles and were grouped together under the category ‘‘other’’. All pairwise comparisons of overall support use (Table 3) and almost all individual comparisons of support use behavior yielded significant differences among age categories (Table 4). Adults utilized the largest supports, boughs (32.1 %) considerably more frequently than did subadults (18.6 %) and juveniles (19.4 %). Branch use was significantly different among individuals of all age categories, with the frequency being largest for subadults (64.5 %), followed by juveniles (57.9 %) and adults (54.0 %). Twig use differed significantly among the age categories, with the percentage decreasing from juveniles (13.5 %) to subadults (8.2 %) and to adults (4.3 %).
Postural behavior
Discussion
Sitting was by far the most common posture (89.5–92.5 %) for individuals in all age categories; percentages of prone lie, recline, and stand were smaller (Table 2). Overall
I found that C. a. palliatus activity budgets and support use differed substantially among age categories whereas postural and locomotor behavior were, in general, consistent.
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Primates (2015) 56:183–192 Table 4 Pairwise comparison of individual activity, positional behavior, and support use categories for the three age classes of C. a. palliatus
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Age class Adult vs. subadult
Subadult vs. juvenile
Adult vs. juvenile
Activity budget Feed
Z = 3.8, P \ 0.01
ns
Z = 3.9, P \ 0.01
Forage
Z = 3.1, P \ 0.01
ns
Z = 4.2, P \ 0.01
Move
Z = 3.6, P \ 0.01
Z = 4.0, P \ 0.01
Z = 10.4, P \ .0.01
Rest
Z = 8.8, P \ 0.01
ns
Z = 9.7, P \ 0.01
Social
Z = 7.1, P \ 0.01
Z = 6.3, P \ 0.01
ns
Locomotor behavior Quad. Walk
ns
ns
Z = 2.5, P \ 0.01
Bound
ns
ns
Z = 2.8, P = 0.01
Climb
Z = 2.5, P \ 0.01
ns
Z = 4.1, P \ 0.01
ns
ns
ns
Leap Postural behavior Sit
ns
ns
Z = 3.7, P \ 0.01
Prone lie
ns
ns
Z = 2.8, P \ 0.01
Recline
Z = 2.0, P = 0.04
Z = 2.1, P = 0.04
Z = 4.7, P \ 0.01
Support use Bough
Z = 9.8, P \ 0.01
ns
Z = 11.5, P \ 0.01
Branch
Z = 7.0, P \ 0.01
Z = 3.9, P \ 0.01
Z = 3.4, P \ 0.01
Twig
Z = 5.9, P \ 0.01
Z = 4.7, P \ 0.01
Z = 14.3, P \ 0.01
These results emphasize that positional behavior competence develops relatively quickly during the course of a primate’s life. Activity budgets were highly variable among age categories. Most notably, adults rested more and moved less than subadults and juveniles. A similar trend has been described for other primate species (Rose 1977; Wells and Turnquist 2001; Prates and Bicca-Marques 2008), because younger individuals typically spend more time exploring their environments, playing, and socializing with one another than do adults (Jansen and van Schaik 1993). The high frequency of socializing (i.e., 7.6 %) reported for subadult C. a. palliatus can probably be attributed to: (1) frequent grooming of higher ranking adult individuals, and (2) learning to care for infants—especially by subadult females—as aunting behavior is a characteristic of colobine monkeys (Poirier 1968; Oates 1977; McKenna 1979). Time spent feeding among individuals in the different age categories may be misleading. Although adults spent the least amount of time feeding, it is reasonable to predict they actually consume more food than smaller-bodied subadults and juveniles. Data on dietary composition, food intake, and ingestion rate among the different age categories are required to clarify this issue (Nakagawa 2009). Locomotor profiles of adults differed significantly from those of juveniles; however, all other pairwise comparisons of overall locomotor profiles were not significant. It is well documented that climbing is particularly difficult to define
and differentiate from other locomotor modes, for example quadrupedal walking (Hunt et al. 1996; Dagosto and Gebo 1998). Nonetheless, the higher frequency of climbing among juveniles was probably related to their proclivity to move through and forage from thin terminal branches whereas adults were more limited to walking on and feeding from larger and more stable supports. Juveniles also bounded significantly less frequently than did adults and subadults. Although its adaptive significance is not well understood, this quadrupedal gait is observed for all extant black and white colobus monkey species (Morbeck 1976; Rose 1979; Gebo and Chapman 1995b; McGraw 1998a; Dunham and McGraw 2014) and was probably important in the evolution of the Colobus genus. This locomotor behavior is not practiced by closely related olive colobus (Procolobus spp.) or red colobus monkeys (Piliocolobus spp.) (Gebo and Chapman 1995b; McGraw 1998a), although it has been observed among a handful of small-bodied primates (Garber 1991; Rosenberger and Stafford 1994; Preuschoft et al. 1996) and is more common among rodents and small carnivores (Hildebrand 1977). Because bounding is believed to involve greater hindlimb propulsive forces and higher impact forces on the forelimb compared with other quadrupedal walking and running modes (Morbeck 1976; McGraw and Daegling 2009), it is likely that this gait is facilitated by mature fullydeveloped musculature and joint complexes. This idea has yet to be tested, however; I hypothesize that lower the
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frequency of bounding among juvenile C. a. palliatus is associated with the development of musculoskeletal anatomy incapable of withstanding the forces typically associated with bounding. If bounding does indeed provide some selective advantage in Colobus spp. (e.g., faster or more energy-efficient gait), it makes sense that individuals adopt this gait more frequently in subadult and adulthood as their musculoskeletal anatomy develops and is capable of withstanding forces associated with bounding. Clearly this gait and its adaptive context demand additional investigation. Future studies quantifying the force transferred during different locomotor behavior (Kimura 1992) and morphometric analysis of the skeleton among different age classes are needed to test this hypothesis. That the primary gap-crossing behavior of C. a. palliatus (i.e., leaping) did not differ with age is surprising. Fleagle and Mittermeier (1980) hypothesized that larger animals encounter fewer gaps in any given habitat and thus should leap less than smaller-bodied primates because they can cross such discontinuities by use of energetically more efficient and less risky behavior (e.g., bridging and climbing). This prediction was supported by their study of a primate community from Surinam but subsequent evidence has been less conclusive (Gebo and Chapman 1995b; McGraw 1998a; Youlatos 1999). Given that my study found no differences between the frequency of leaping, it is apparent that body size alone is not a reliable predictor of leaping behavior (Gebo and Chapman 1995b; McGraw 1998a). There are several possible explanations for the discrepancies among these studies. First, Fleagle and Mittermeier (1980) studied a community of New World primates including species with prehensile tails (i.e., Alouatta seniculus and Ateles paniscus). This feature is known to greatly facilitate bridging behavior to an extent not observed for Old World monkeys. Gebo and Chapman (1995b) and McGraw (1998a) found no relationship between body size and leaping frequency among members of primate communities in Uganda and Coˆte d’Ivoire, respectively; however, when restricting the comparison to colobines only, McGraw (1998a) found support for Fleagle and Mittermeier’s (1980) prediction: the smallest colobine (Procolobus verus) leaped significantly more frequently than did larger red colobus monkeys (Piliocolobus badius) and the largest of the three species, black and white colobus monkeys (Colobus polykomos). Even though the frequency of leaping did not differ among age categories in this study, it is likely that the larger body size and developed musculature characteristic of adults enables them to leap greater distances than subadults and juveniles. Although Colobus spp. are notorious for the their spectacular leaping ability (Morbeck 1976), Gebo and Chapman (1995b) found that almost all adult C. guereza leaps (i.e., *85 %) covered only short distances
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of two body lengths or less. Thus, even though juveniles may be unable to achieve the maximum leaping distances of adults, they are likely to be capable of making the far more common short-distance leaps. This could explain why leaping frequencies were not significantly different among adults, subadults, and juveniles in this study; however, future studies are required to elucidate the context of leaping, and distance spanned, for different age categories of C. a. palliatus. Although body size must surely have some effect on whether an animal chooses to leap or use another locomotor mode to cross a canopy gap, it is likely that other factors, for example foraging behavior, strata use, predation pressure, and phylogeny are of equal, if not greater, importance in affecting leaping behavior. As observed in other studies of Colobus spp. (Mittermeier and Fleagle 1976; Morbeck 1977, 1979; Rose 1979; Gebo and Chapman 1995b; McGraw 1998b), sitting constituted the predominant postural behavior for each age category and was the most common posture during feeding and resting. There were, however, statistically significant differences between the frequencies of other postures, particularly for adults and juveniles. Different postural behavior is likely to be related to different activity budgets. Adults engaged in more frequent and prolonged rest periods, with more instances of prone lie and recline, than more active and playful juveniles. It is likely that these sprawled positions (i.e., prone lie and recline) aid thermoregulation and/or digestion (Dasilva 1993) and that individuals of all ages thermoregulate and achieve digestion in different ways in relation to body size and metabolic requirements. Research has demonstrated that as primate body size increases, gut size and volume become proportionately larger (Chivers and Hladik 1984). Although relationships among body size, gut size, and diet are typically used to explain interspecific differences between primate food choice and food processing behavior, it is likely that these relationships can also be used to understand intraspecific differences between diet with regard to age and development. For instance, Hanya (2003) found that adult Japanese macaques (Macaca fuscata) consumed larger quantities of fibrous plant material than did juveniles. Particularly for highly folivorous colobine monkeys, it is possible that the larger digestive anatomy of adults combined with fully developed dentition and greater inactivity enable them to digest a more fibrous diet compared to that of juveniles. Support use varied greatly among all age categories. Almost all G-tests of overall support profiles and Z-tests of individual support use comparisons yielded significant differences. In general, adult colobines are limited to and choose to utilize larger supports to maintain stability and balance (McGraw 1998a). Subadult and juvenile C. a. palliatus were more diverse in their support use, probably because they are smaller and nimble enough to maneuver
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on thinner, more flexible supports. In some ways, juvenile C. a. palliatus support use was more like that of similarly sized adult Cercopithecus spp. (McGraw 2000), emphasizing the link between body size and support use. Although strata use is not reported in this study, individuals in a given group usually moved cohesively and occupied a common forest stratum at any given time. Thus, it is unlikely that support use differences are an artifact of idiosyncrasies in strata use among age categories. Previous research has demonstrated that locomotor and postural behavior are largely similar among different age and sex categories of a particular species despite differences in body size and the frequency of some individual locomotor behaviors (Doran 1992, 1997; Inouye 1994; Wells and Turnquist 2001; Thorpe and Crompton 2005; Workman and Covert 2005; Bezanson 2006, 2009, 2012; Lawler 2006; Prates and Bicca-Marques 2008). For example, locomotor behavior or support use were not significantly different for yearling and adult sifakas (Propithecus verreauxi verreauxi) (Lawler 2006). Juvenile capuchin monkey (Cebus capucinus) positional behavior profiles were indistinguishable from those of adults (Bezanson 2009). Juvenile chimpanzee (Pan troglodytes) positional behavioral profiles were remarkably similar to those of adults (Doran 1992). Similarly, orangutan (Pongo pygmaeus abelii) locomotor profiles were mostly consistent for almost all age and sex categories (Thorpe and Crompton 2005). In contrast, positional behavior of some species including mountain gorillas (Gorilla gorilla beringei), rhesus macaques (Macaca mulatta), and howler monkeys (Alouatta palliata) were less consistent throughout ontogeny (Doran 1997; Wells and Turnquist 2001; Bezanson 2006, 2009, 2012). Factors which might account for this apparent discontinuity in results are unknown. First, it is possible that methodological inconsistencies in the number of recognized age categories among studies contribute to whether differences in positional behavior are revealed. For example, Doran (1997) compared mountain gorilla positional behavior among 13 different age categories (compared with three in this study) including six discreet infant stages. Virtually all of the reported significant differences in locomotion were found when behavior was compared among individuals in different infant age categories. Mountain gorillas were generally adult-like in their positional behavior by 4 years of age (Doran 1997). Infant C. a. palliatus positional behavior was not recorded, because only one of the study groups contained an infant and this infant was only present for part the study period. Nonetheless, this infant C. a. palliatus typically engaged in slow and shaky quadrupedal walking and abbreviated leaping when moving independently through the canopy, although these data were not quantified or recorded. Similarly, several studies have recorded dramatic discrepancies
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between infant and adult positional behavior (Kimura 1987; Vilensky and Gankiewicxz 1989; Doran 1992, 1997; Wells and Turnquist 2001; Bezanson 2006; Prates and Bicca-Marques 2008). This is not surprising given that infants are usually less coordinated and often rely on clinging to other individuals during travel (Vilensky and Gankiewicxz 1989; Wells and Turnquist 2001). As they progress through infancy and become more independent, primates refine and hone their locomotor skills. This was reflected in my study. For some primate species, however, there are significant differences between the positional behavior of juveniles and adults. This can partially be explained by the so called ‘‘golden age’’ of positional behavior observed for juveniles (Dunbar and Badam 1998: p. 543), because they have relatively well-developed motor skills and more flexible joints without the larger body size that constrains adults. This, combined with juveniles’ proclivity to explore and play, often results in greater diversity of positional behavior. For instance, Workman and Covert (2005) observed several types of positional behavior among juveniles of three species of Asian colobines that were not seen among adults, and the juveniles used suspensory locomotor behavior significantly more frequently than adults. My study corroborates these results—juvenile C. a. palliatus had a more diverse locomotor repertoire (behavior reported in the ‘‘other’’ category) and, unlike adults, occasionally used bimanual suspensory locomotion. That species achieve adult-like positional behavior profiles at different stages of ontology is clearly demonstrated by Bezanson’s (2006, 2009, 2012) extensive research on sympatric capuchin monkeys (Cebus capucinus) and howler monkeys (Alouatta palliata). Bezanson (2009, 2012) and Bezanson and Morbeck (2013) highlight the apparent disconnect between life history variables and the ontogeny of positional behavior. Compared with A. palliata, C. capucinus are characterized by a generally ‘‘slower’’ life history strategy (i.e., older age at first reproduction, slower brain development, longer lifespan (Ross 1991). Thus, one could reasonably predict that capuchin monkey positional behavior competence would take a substantial time to develop over the course of a prolonged juvenile period. Instead, C. capucinus acquire an adult-like repertoire of positional behavior by 6 months of age, approximately six and a half years before sexual maturity (Bezanson 2009). Conversely, A. palliata, are characterized by a ‘‘faster’’ life history (i.e., younger age at first reproduction, shorter interbirth interval) than capuchin monkeys but do not achieve an adult-like positional behavior profile until 24 months of age (Ross 1991; Fedigan and Rose 1995). This disassociation between life history and ontogeny of positional behavior is not well understood, but it is likely that interactions among several
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other variables (e.g., foraging behavior and efficiency, body size, predation pressure, and musculoskeletal development) may exert stronger pressures on positional behavior (Cant 1992; Jansen and van Schaik 1993; Wells and Turnquist 2001). By the time individuals reach the subadult or adolescent stage, the positional behavior repertoires of virtually all primate species studied to date are indistinguishable from those of their adult counterparts. Morphological constraints associated with body size and limb anatomy are likely to be the primary reason for these similar positional behavior profiles. Researchers have examined a variety of age-related changes in primate behavior. This study adds to a growing, but still fledgling, literature on the ontogeny of primate positional behavior. Examining how positional behavior varies with age provides insight into a species’ behavioral ecology and helps us better understand relationships between behavior and a given anatomy. Locomotor and postural behavior were generally consistent across three age categories of C. a. palliatus despite markedly different body size and some aspects of behavior. These findings emphasize that some measures of behavior (e.g., activity budgets) vary among individuals at different life stages and in association with changes in such factors as physical growth and maturation, metabolic requirements, mental development, and social status. Given that the positional behavior of individuals of different ages was remarkably similar despite major support use idiosyncrasies, I stress that positional behavior is largely conserved intraspecifically and strongly constrained by morphology. There is likely to be strong selective pressure on achieving adultlike locomotor and postural competence early during the juvenile period in order to escape predators and, for arboreal primates like colobus monkeys, maintain stability and avoid falling from the canopy (Jansen and van Schaik 1993). It is hypothesized that reported disparities in the frequency of some locomotor behaviors, for example bounding, can be explained by the different musculoskeletal features of adults and juveniles. To test this hypothesis, future studies are required to examine the ontogeny of bounding among other primates and mammalian taxa (Hildebrand 1977; Garber 1991; Rosenberger and Stafford 1994; Preuschoft et al. 1996) and/or experimentally examine the kinematics of bounding among different age categories of black and white colobus monkeys (Hanna and Schmitt 2011). Acknowledgments This material is based on work supported by the National Science Foundation Graduate Research Fellowship under grant no. 2012136655, The Earth and Space Foundation, The Primate Society of Great Britain, The Ohio State University, and Sigma Xi. I acknowledge the Kenyan government for permission to conduct this
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Primates (2015) 56:183–192 research. Thanks to Pam Cunneyworth, Andrea Donaldson, and Keith Thompson of Colobus Conservation for providing logistical support for this study. Thanks to Bakari Mnyenze, John Ndege, and Paul Opere for their assistance with data collection. I thank Scott McGraw and three anonymous reviewers for their comments on earlier versions of this manuscript.
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