1Bipedal behavior has been documented for several non-human primate species in natural environments. It has often been studied to better understand the evolution of hominin bipedalism, even though bipedal posture and gait in non-human primates differ from bipedalism in humans, and likely differ from those of the earliest ancestral human bipeds. In the laboratory setting, studies have determined the anatomical and biomechanical framework within which non-human primates achieve bipedal postures and movement (Schmitt, 2003; Druelle & Berillon, 2014). The adaptive significance of bipedal behavior has commonly been related to the acquisition and transport of food items, as well as specific social and environmental contexts that require orthograde postures and/or the free use of the forelimbs (Fleagle, 2013).
2Due to their generalized quadrupedal form, behavioral variability, propensity for hard object feeding, and widespread geographical range, capuchins, and in particular robust (or tufted) capuchins (Sapajus spp.), have been used as model primate species in which to examine questions concerning the evolution of feeding systems in hominids, such as how an otherwise quadrupedal primate can use bipedal behavior to access food items. (Ford & Hobbs, 1996; Kinzey, 1974; Wright et al. 2015; Wright, 2005; Laird et al. 2020). Bearded capuchins (Sapajus libidinosus), the subject of this study, live in seasonally arid environments, and frequently use terrestrial parts of their environment (Visalberghi & Fragaszy, 2013; Visalberghi et al. 2007). Adult bearded capuchins use bipedal behaviors, such as bipedal walking (1% of positional behaviors), bipedal standing (4.1% of positional behaviors), and bipedal crouching (12.1% of positional behaviors), in both arboreal and terrestrial natural settings, primarily during feeding, foraging including using stone hammers and anvils to open nuts, and transporting food items or tools (Wright et al. 2019). Because of these behaviors, bearded capuchins have served as a model species in which to examine the kinematic and anatomical underpinnings of bipedalism. Kinematic studies of Sapajus have been undertaken both in natural environments and laboratory settings. For example, in a kinematic study of wild bearded capuchins using bipedal locomotion while transporting stones to anvils (to crack nuts), Duarte et al. (2014) showed that during stone transport, bearded capuchins moved faster, and used a higher duty factor than when moving bipedally when not carrying a stone. In another study, Liu et al. (2009) compared bearded capuchins’ way of lifting heavy hammer stones to crack palm nuts to powerlifting in humans, in that the trunk is erect during lifting and both feet may leave the ground during the apex of the lift. Laboratory studies of the kinematics of brown capuchins (Sapajus apella), have shown that, while similar to the facultative bipedalism demonstrated by other non-human primates, capuchins include a short aerial phase when locomoting bipedally that can be classified more as running than as walking (Demes, 2011; Demes & O’Neill, 2013). Studies such as these have demonstrated how an arboreal quadruped with a more generalized postcranial anatomy is able to perform bipedal postural and locomotor behaviors under conditions that may have driven selection for obligate bipedalism in humans (see Harcourt-Smith, 2007 for a review).
3In natural environments, bipedal behavior comprises a relatively small fraction of the total positional behavioral repertoire of habitually quadrupedal haplorhine primate species (e.g., see review of catarrhine studies by Druelle & Berillon, 2014, as well as Wright et al. 2019; Falótico et al. 2016; Machnicki et al. 2016; Cant et al. 2001; Youlatos, 1998; Fontaine, 1990; and Mittermeier, 1978 for examples of platyrrhine bipedal behavior in the wild). Bipedal behavior in non-human primates occurs during foraging (Biondi, 2010; Wright et al. 2019; ), object transport (e.g., Rose, 1974; Carvalho et al. 2012; Visalberghi et al. 2009; Falotico et al. 2016; Biondi, 2010; Wright et al. 2019), tool use (e.g., Fragaszy et al. 2004), the use of certain types of substrates or other habitat features (e.g. Berillon et al. 2011; Wright et al. 2019, Falotico et al. 2016), social interactions, and, particularly in the case of infants and juveniles, play (e.g., Biondi, 2010; Rose, 1976; Fontaine, 1994). Higher frequencies of bipedal behaviors have been reported for infants and juveniles compared to adults in non-human apes, baboons, and macaques (see again Druelle & Berillon, 2014). For platyrrhine species, less is known about how bipedal posture and locomotion differ between adults and youngsters. Biondi (2010) reports that overall, juvenile bearded capuchins and adults shared similar positional behaviors and use of substrates except during play, when juveniles adopted more varied positions than adults. Juvenile bearded capuchins used suspensory postures more than adults and adults more quadrupedal locomotion than juveniles during feeding. Bezanson (2009) reports that, overall, juvenile white-faced capuchins (Cebus capucinus) show a more diverse pattern of positional behaviors than adults and their positional behavior resembles an adult pattern by six months of age. In Bezanson’s study, the youngest category of juvenile used the bipedal posture “flexed bipedal stand” slightly more than older juveniles or adults (2.3% versus 1.6% and 1.9%, respectively). No other bipedal behaviors were reported in this study.
4Here, we expand on the previous studies of bipedal postures and locomotion with Sapajus mentioned above by providing a rich data set in terms of number of individuals, age distribution, and diversity of substrates and activities, drawn from the dataset presented by Biondi (2010). Broad analyses of these data for adults with respect to positional behavior have been presented previously (Wright et al. 2019). In this study, we provide a limited, but focused, look at the main elements of bipedal behavior in adults gleaned from the dataset used in the previous paper, expand the data set to include immatures, and provide additional context for the occurrence of this relatively rare behavior in both adults and immatures. In a subsequent report we will present ontogenetic analyses of the full positional and locomotor repertoire of these monkeys.
5This study was undertaken at Fazenda Boa Vista (FBV). The site is privately owned land in the Cerrado-Caatinga ecotone in Gilbués, Piauí, Brazil (9o 39’S, 45o 25’W; Howard et al. 2012; Oliveira & Marquis, 2002; Visalberghi & Fragaszy, 2013). The site of this study is described in more detail in Wright et al. (2019). Briefly, the vegetation is characterized by open woodland. The topography is a sandy plain punctuated by sandstone ridges, pinnacles, and mesas rising in sheer cliffs 30 – 100 m above the plain. The talus of the ridges contains sandstone boulders, and ephemeral streams carry smaller stones, many of them ironstone, siltstone, and quartzite, down the slopes from the eroding cliffs into the plain, which constitutes a shallow, broad valley. A wetland area with slow-flowing ephemeral stream and riparian vegetation occupies the center of the valley. The substrates used by the monkeys for locomotion include the sandy soil, boulders and cliff faces, shrubs, and vines (particularly near the wetland area), and deciduous trees rising to about 20 m maximum, some of which have lateral branching patterns. The canopy is relatively open even in wooded areas.
6Sixteen wild adult bearded capuchins (nine females and seven males, 15 years and older) and 16 juvenile bearded capuchins (6 females and 10 males), ranging in age from 3 months to 51 months (4.2 years) old, from two habituated groups were observed from October 2008 to September 2009. The monkeys inhabit the same environment, and their home ranges partially overlap. Records of births, immigrations, and disappearances for the two bearded capuchin study groups at Boa Vista have been kept by the research team since 2005, allowing accurate age assignments for all juveniles and infants, and reliable age estimates for several adults included in this study. Adult individuals for which year of birth was unknown were assigned the age of 180 months (15 years) (Fragaszy et al. 2004). Juvenile individuals were assigned age based on known birth month and year (Table 1).
7Each group was followed for 5 days per month. Data were collected during three separate observational periods per day (morning, mid‐day, and afternoon). Instantaneous focal animal sampling (Altmann, 1974) was used to collect data on activity state, positional behavior, and substrate use every 15 s for 2 min (eight consecutive records) for individually identified subjects (Table 1). During each period per day, individuals were each observed for a maximum of three 2‐minute samples each, allowing for a maximum of 24 instantaneous records per time period (72 records per individual, per day). This focal animal timing strategy helps to randomize data collection, prevents over-sampling of particular individuals, and allows for a more evenly distributed number of observations per individual. The data presented here, consisting of 2,209 observations, are a subset of a larger dataset; this subset includes records of activity state, positional behavior, and substrate use during bipedal behaviors only (Tables 1 & 2).
Table 1
Number of study subjects and observations by age group.
Table 2
Description of Activity, Bipedal Behaviors, Substrates, and Tail Use recorded in this study.
8Individuals were grouped into 6 age groups based on the individual’s age at the start of data collection. Juveniles (the birth dates for all of which were known to within 2 months) were classed by year up to 5 years. All individuals over 5 years were considered adults and for purposes of graphing assigned an age of 15 years: <1 year old (3-<12 months), 1-<2 years old (11-<24 months), 2-<3 years old (24-<36 months), 3-<4 years old (36-<48 months) and 4-<5 years old (48-<60 months), and adults (180 months) (Table 1). Chi-square (χ2) tests of independence were used to examine the relationship between age (6 groups) and patterns of bipedal behavior (crouch, stand, locomotion), activity (forage, locomote, play, other), substrate use (arboreal, terrestrial, conspecific), and tail use (grasp, touch, up). Chi square tests were performed on the frequency counts. Cramér’s phi (ϕ) was calculated to determine effect size. Figures and text present the data as percentages of records within age groups for ease of comparison across age groups (as age groups had variable total counts of bipedal behavior; see Table 1). In addition, we used Pearson’s correlation coefficients to determine whether bipedal behavior was associated with age.
9Considering the entire positional repertoire of bearded capuchins for all age classes pooled, bipedal behaviors (all types combined) comprise 10.9% of their total positional behavior repertoire, or 2,209 observations out of a total of 20,256 total observations of positional behavior. To reiterate, here we report the results of a focused analysis of those 2,209 observations of bipedal behavior.
10From infancy to adulthood, bearded capuchins showed similar patterns of bipedal behaviors with bipedal crouch being the most common bipedal behavior exhibited (72.0% of all bipedal behaviors observed for pooled age classes), followed by bipedal stand (24.9% all bipedal behaviors observed for pooled age classes). Bipedal locomotion happened rarely (3.1% of all bipedal behaviors observed for pooled age classes). Chi-square (χ2) test of independence revealed that distribution of the three forms of bipedal behavior did not vary across age groups (χ2 (10) = 11.77, ϕ=0.05, p=.301), with average values per age group for bipedal crouch ranging from 67.6% to 81.8%, bipedal stand from 15.9% to 27.3%, and bipedal locomotion from 2.3% to 5.1% (Figure 1).
Figure 1
Comparison of bipedal behaviors by age group. Colored bars represent proportion of observations for each category, for each age group.
11Although forms and patterns of positional behavior do not vary from infancy to adulthood, a comparison of individuals ranging in age from 3 months to 51 months (essentially, all immatures or juveniles) with all adults (individuals or unknown exact birthdate but determined to be fully mature adults of at least 180 months in age) reveals that juveniles are more variable across individuals for each bipedal behavior and overall, in accord with changes in age. Coefficients of variance for juveniles ranged from 59 to 102; for adults, from 38 to 72. Specifically, values for juveniles were, for bipedal crouch: mean = 8.30, SD = 4.63, CV = 59; for bipedal stand: mean = 2.68, SD = 1.71, CV = 63; for bipedal locomotion: mean = 0.39, SD = 0.40, CV = 102; and for all bipedal behaviors pooled: mean = 11.52, SD = 6.24, CV = 54). Equivalent values for adults (individuals at least 180 months in age) were, for bipedal crouch: mean = 7.92, SD = 3.01, CV = 38; for bipedal stand: mean = 2.77, SD = 1.04, CV = 38; for bipedal locomotion: mean = 0.30, SD = 0.21, CV = 72; and for all bipedal behaviors pooled: mean = 10.99, SD = 3.17, CV = 38.
12For juveniles from age 3 months to 51 months, bipedal behavior is moderately positively correlated with age (Pearson correlation results: bipedal crouch, r(14) = +.69, p<.01; bipedal stand, r(14) = - .60, p<.02; bipedal locomotion, r(14) = +.61, p<.02; bipedal behaviors pooled, r(14) = +.70, p<.01). Adults’ bipedal behavior appears to be randomly distributed across the three bipedal behavior categories (bipedal crouch, bipedal stand, and bipedal locomotion) (i.e., Pearson correlations (n = 16; df = 14) across individuals of these behaviors with each other ranged from -.07 to +.26).
13For all age groups, bearded capuchins used bipedal behavior most frequently while feeding or foraging. However, chi-square (χ2) test of independence suggested that age groups used bipedal behaviors in different proportions in some other activities. Compared to other age groups, bearded capuchins less than 12 months old used bipedal behaviors during play and during activities scored as “other” more frequently than other age groups (χ2 (15) = 211.36, ϕ=0.18, p<.001) (Figure 2). Play and other activities constituted a greater proportion of the daily activity budget for the youngest age group compared to the other groups (56.8% of records, compared to 5.3% – 13.0% for all other age groups).
Figure 2
Comparison of activity states during bipedal behavior by age group. Colored bars represent proportion of observations for each category, for each age group.
14Bearded capuchins used bipedal behaviors more frequently in arboreal settings than in terrestrial settings (percentage of bipedal records = 61.4% arboreal vs 38.1% terrestrial). Bearded capuchins less than 12 months old (which are frequently carried by adults or older juveniles) sometimes used bipedal postures while supported by another (standing on the other monkey’s back), accounting for <1% of bipedal records. Monkeys older than 12 months never did this (χ2 (10) = 218.55, ϕ=0.22, p<.001) (Figure 3).
Figure 3
Comparison of substrate use during bipedal behavior. Colored bars represent proportion of observations for each category, for each age group.
15Across all age groups, bearded capuchins nearly always had their tail grasping or in contact with a substrate while they performed bipedal behaviors (85.4 % of bipedal records) (χ2 (10) = 14.82, ϕ=0.06, p=.139; Figure 4). Bearded capuchins used their tails to grasp proportionally more frequently on arboreal substrates (37.7% of arboreal records) than on terrestrial substrates (8.9% of terrestrial records). Conversely, they touched their tails to the substrate (without grasping or gripping) proportionally more frequently on terrestrial substrates (73.1% of bipedal records on terrestrial substrates) than on arboreal substrates (49.7% of bipedal records on arboreal substrates). The monkeys did not contact any surface with their tails on 12.6% of records on arboreal substrates and 18% of records on terrestrial substrates. Monkeys were observed to touch their tails to the surface 13 times during bipedal locomotion (2.0% of records of bipedal locomotion). A detailed analyses of how the monkeys used their tails while moving and while stationary will be presented elsewhere.
Figure 4
Comparison of tail use during bipedal behavior. Colored bars represent proportion of observations for each category, for each age group.
16Bipedalism (bipedal posture and locomotion) in non-human primates, while fairly well-documented for African and Asian monkeys and apes in both arboreal and terrestrial settings (Druelle & Berillon, 2014), is a relatively rare behavior, and considered to be facultative. It is typically associated with foraging, feeding, and object transport, but also occurs during social and play activities, as well as predator avoidance. Robust capuchins (Sapajus spp.) are a generalized arboreal quadruped known to use bipedal behaviors in the wild, primarily in association with the same activities reported for other species: feeding, foraging, and transporting objects (Wright, 2019; Falótico et al. 2016; Youlatos, 1998). In addition, we previously reported (Wright et al. 2019) that bipedal behavior in adult bearded capuchins (S. libidinosus) constituted about 17% of adults’ positional time budget, occurred most often on terrestrial substrates, and was dominated by bipedal crouching, with bipedal standing and bipedal locomotion happening infrequently. Here, we have focused our analyses on the spectrum of bipedal behavior in all age classes, and added observations of tail use during bipedal behavior, in order to better understand the context in which bipedal behaviors occur in bearded capuchins. Studies of positional behavior that include animals younger than adults are relatively rare. Our study has afforded a unique opportunity to examine bipedal behavior and the contexts in which it occurs in wild animals of all ages in one species of South American primates.
17The monkeys that we studied were seen using bipedal postures and behaviors in 10.9% of their samples, and adults did not differ from juveniles in this variable. Bipedal crouch is the dominant bipedal behavior used by all of the bearded capuchins at FBV, followed by bipedal stand (72% and 24.9% of all bipedal behavior, respectively). Bipedal crouch, as defined in this study, is comparable to the behavior “bipedal crouch plus tail” defined by Garber & Regh (1999), with the exception that we include non-grasping tail use, as well as grasping tail use in our definition. The bearded capuchins in this study were observed using bipedal crouch in both arboreal and terrestrial settings, and thus, compared to white-faced capuchins, which use primarily arboreal settings, the ecological relevance of tail use may be different. Bearded capuchins, for example, forage extensively on the ground and when adopting bipedal postures will either hold their tail up (typically when locomoting), touch the ground with their tail (for example, when standing bipedally), but they do not always use it to grasp a nearby object or branch for support (see below).
18Age classes did not differ in patterns of bipedal behaviors and substrates used, despite age-related differences in body size (Fragaszy et al. 2016). This may reflect that juvenile monkeys feed on the same foods as adults (Chalk et al. 2016); thus, they are foraging and processing foods in the same places as adults. Even bipedal locomotion, arguably the most challenging bipedal behavior due to the requirements for dynamic balance while moving, was performed at similar rates by monkeys of all ages. The only differences in behavior across ages that we found concerned the youngest age group (3 - 12 months). This group used by bipedal postures in play more than other groups, as well as other behaviors not much performed by adults (such as rolling supine on the ground, and full suspension by one hand). For example, bearded capuchins from 3-12 months old occasionally used older individuals as a substrate for their bipedal activity; older individuals never did so.
19There are relatively few studies that have examined ontogenetic variation in positional behavior in free-ranging non-human primates, but for those that have reported bipedal behavior, bipedalism appears to be more prevalent in infants and juveniles (e.g., Doran, 1992; 1997; Wells & Turnquist, 2001; Druelle & Berillon, 2013; Sarringhaus et al. 2014). Thus, the finding that bearded capuchins show no significant age-related differences in the proportional frequency or in the patterns of bipedal behaviors in this study is interesting. The findings suggest that bipedal activity plays a similar role in the lives of bearded capuchin monkeys across the life span.
20Monkeys used their tails to touch or grasp the substrate for most records of bipedal crouch and stand both in arboreal and terrestrial settings. Bipedal locomotion occurred almost exclusively on terrestrial substrates, and typically without support from the tail (note that the tail would drag if it touched the ground during locomotion). The absence of information about body position afforded by the tail touching the surface may add to the challenge to balance experienced during bipedal locomotion on terrestrial substrates. Thus, it is surprising that bipedal locomotion constituted an equivalent proportion of bipedal records for young monkeys as for adults. For this and many other reasons, the onset of bipedal locomotion warrants further investigation. Longitudinal studies would be most useful for this purpose.
21Bearded capuchins held their tail up and away from contact with any surface slightly more often while on terrestrial substrates than arboreal substrates. Across all age classes, bearded capuchins used their tails to touch more often than to grasp a surface, even in arboreal settings. However, they used the tail to grasp proportionally more frequently while in an arboreal setting than in a terrestrial setting. This pattern makes sense given that using the tail to touch or to grasp both aid in maintaining secure balance but grasping with the tail provides mechanical aid in maintaining one’s position, whereas touching does not. Falling is a greater risk while in a tree than on the ground. In this report, we have not examined whether the sizes or types of arboreal substrates were associated with different proportions or patterns of tail use, and this would be worth further investigation. Garber & Regh (1999) note that white-faced capuchins (Cebus capucinus) wrap their tails around nearby, supporting branches during bipedal crouching (i.e., “bipedal crouch plus tail”) during foraging and feeding, and that during this posture, their tails are held in tension. They report that white-faced capuchins use their tails as an anchor, or third grasping appendage, 54.4% of the time when feeding on fruits and 37.7% of the time when foraging for or feeding on insects and vertebrates, and particularly during bouts of destructive foraging. In Garber & Regh’s study, the authors focused on how white-faced capuchins used their tail as a support during above- and below-branch positional behaviors but did not report on terrestrial behavior or non-grasping uses of the tail in white-faced capuchins. Bearded capuchins’ reliance on the tail to contact a surface, without actually grasping it, may be evidence that capuchin monkeys also use the tail for dynamic touch (sensu Turvey, 1996) to aid in maintaining balance and orientation, as touching a firm substrate with the hand aids humans to maintain balance during resting bipedal stance (e.g., Clapp & Wing, 1999) and when balance is challenged (Dickstein & Laufer, 2004; Martinelli et al. 2015). In any case, further investigation is needed to determine if capuchins use the tail less or differently than reported here when they use quadrupedal postures, that are presumably more stable than bipedal postures.
22Here we have examined ontogenetic patterns in a specific positional behavior, bipedalism, in bearded capuchins and attempted to place this relatively rare behavior in the context of activity and substrate use. We did not identify differences in patterns of bipedal behavior across ages in this species, in keeping with findings about wedge-capped capuchins (Cebus olivaceus) and white-faced capuchins (C. capucinus), neither of which showed significant age-related variation in pattern of positional behavior [Wright 2003, 2005 (PhD thesis); Bezanson 2006a, 2006b, 2009]. However, previous studies have reported that juvenile brown capuchins (S. apella) differed markedly in patterns of positional behavior compared to adults [Wright 2003, 2005 (PhD thesis)]. Specifically, juvenile brown capuchins climbed and leapt more than adults. However, Wright [2003, 2005 (PhD thesis)] did not observe bipedal behavior in that study, which was conducted in a rainforest environment, and did not know the exact ages of individuals younger than adults. In any case, the difference in findings across the two studies may hint at the influence of habitat type on the use of bipedal behaviors and/or the importance of bipedal behavior for bearded capuchins, which live in the relatively drier Cerrado-Caatinga environment, compared to brown capuchins. These varied findings warrant that we cast our net wider and examine the full range of positional behavior in robust capuchins across the life span and in varied habitats.
23Finally, although bipedal posture and gait in non-human primates differs from bipedalism in humans, and likely differs from what may have been exhibited by the earliest ancestral human bipeds, understanding the context in which bipedal behavior occurs in living primates, and the activities with which it is associated, may positively impact interpretations of the fossil record. This study provides a non-human primate model that links bipedal behaviors to terrestrial feeding in a relatively dry environment.
24We thank the Oliveira family for permission to work on their land and for logistical assistance throughout the course of this study and acknowledge Luiz Biondi for data collection and collation. The data presented here were collected as part of a larger study that was conducted with permission from the Brazilian National Research Council (CNPq# 002547/2010), Brazilian Institute for Biodiversity Conservation (ICMBio# 28689‐2), the University of Georgia (IACUC protocol # A2007-10178) and the Kansas City University of Medicine and Biosciences Institutional Animal Care and Use Committee (IACUC; Protocol# 2007‐1). This study was funded in part by the University of Georgia and a grant from the National Geographic Society to DF.
25The authors declare that they have no competing interests.