Fig 4 - uploaded by John A. Nyakatura
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-Point diagram of proportion of time spent above 15 m height for both species (S. mystax and L. nigrifrons) studied at the EBQB (each point represents a daily average).
Source publication
Differential habitat use in sympatric species can provide insight into how behavior relates to morphological differences and as a general model for the study of biological adaptations to different functional demands. In Amazonia, closely related sympatric tamarins of the genera Saguinus and Leontocebus regularly form stable mixed-species groups, bu...
Contexts in source publication
Context 1
... mystax was found primarily in the upper and crown forest layers (> 15 m; 79% of all observations), while L. nigrifrons was found in forest layers below 10 m (87% ; Fig. 4). The difference between species in time spent in different forest layers was significant (Wilcoxon rank sum test: W = 79, P < 0.001). ...
Context 2
... mystax was found primarily in the upper and crown forest layers (> 15 m; 79% of all observations), while L. nigrifrons was found in forest layers below 10 m (87% ; Fig. 4). The difference between species in time spent in different forest layers was significant (Wilcoxon rank sum test: W = 79, P < 0.001). ...
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Citations
... Field data have shown that callitrichine monkeys show varied preferences in their jumping repertoire (Berles et al., 2022;Garber, 1991;Garber and Leigh, 2001;Youlatos, 1999) and establish them as a useful evolutionary model to investigate how behavioral differences in jumping performance are reflected in the morphology and species-specific biomechanics of jumping behavior (Berles et al., 2024;Botton-Divet and Nyakatura, 2021). The three species in our performance sample -Goeldi's monkeys (Callimico goeldii), pied tamarins (Saguinus bicolor) and white-fronted marmosets (Callithrix geoffroyi)were chosen to represent a continuum of jumping propensity and relative hindlimb length while simultaneously narrowing phylogenetic diversity. ...
Jumping is a crucial behavior in fitness-critical activities including locomotion, resource acquisition, courtship displays, and predator avoidance. In primates, paleontological evidence suggests selection for enhanced jumping ability during their early evolution. However, our interpretation of the fossil record remains limited, as no studies have explicitly linked levels of jumping performance with interspecific skeletal variation. We used force platform analyses to generate biomechanical data on maximal jumping performance in three genera of callitrichine monkeys falling along a continuum of jumping propensity: Callimico (relatively high propensity jumper), Saguinus (intermediate jumping propensity), and Callithrix (relatively low propensity jumper). Individuals performed vertical jumps to perches of increasing height within a custom-built tower. We coupled performance data with high-resolution μCT data quantifying bony features thought to reflect jumping ability. Levels of maximal performance between species - e.g., maximal takeoff velocity of the center of mass (CoM) - parallel established gradients of jumping propensity. Both biomechanical analysis of jumping performance determinants (e.g., CoM displacement, maximal force production, peak mechanical power during push-off) and multivariate analyses of bony hindlimb morphology highlight different mechanical strategies among taxa. For instance, Callimico, which has relatively long hindlimbs, followed a strategy of fully extending of the limbs to maximize CoM displacement - rather than force production - during push-off. In contrast, relatively shorter-limbed Callithrix depended mostly on relatively high push-off forces. Overall, these results suggest that leaping performance is at least partially associated with correlated anatomical and behavioral adaptations, suggesting the possibility of better inferring performance from the fossil record.
... Several tamarin species live sympatrically in the Amazon basin [25]. By forming "mixed-species groups'' , some tamarins are even syntopic, traveling and foraging together albeit in different forest layers [26][27][28][29]. Because of species-specific preferences for foraging and traveling in different microhabitats, differential leaping behavior has been documented among callitrichid species, too (e.g., [30][31][32][33][34][35]). ...
... This is also the case for two of the focal species of our study. The first, Saguinus mystax, travels primarily in the upper layers of the forest (79% of the time [26]) and uses mostly horizontal supports thinner than 10 cm during locomotion [34], whereas the second, Leontocebus nigrifrons, primarily uses vertical supports of larger diameter in the lower forest layers (87% of the time) [26,[34][35][36][37][38]. For both species studied by Berles and colleagues [26], it was shown that there was a preference for one leaping type regardless of the available supports in the different forest layers. ...
... This is also the case for two of the focal species of our study. The first, Saguinus mystax, travels primarily in the upper layers of the forest (79% of the time [26]) and uses mostly horizontal supports thinner than 10 cm during locomotion [34], whereas the second, Leontocebus nigrifrons, primarily uses vertical supports of larger diameter in the lower forest layers (87% of the time) [26,[34][35][36][37][38]. For both species studied by Berles and colleagues [26], it was shown that there was a preference for one leaping type regardless of the available supports in the different forest layers. ...
Background
Biological adaptation manifests itself at the interface of different biologically relevant ‘levels’, such as ecology, performance, and morphology. Integrated studies at this interface are scarce due to practical difficulties in study design. We present a multilevel analysis, in which we combine evidence from habitat utilization, leaping performance and limb bone morphology of four species of tamarins to elucidate correlations between these ‘levels’.
Results
We conducted studies of leaping behavior in the field and in a naturalistic park and found significant differences in support use and leaping performance. Leontocebus nigrifrons leaps primarily on vertical, inflexible supports, with vertical body postures, and covers greater leaping distances on average. In contrast, Saguinus midas and S. imperator use vertical and horizontal supports for leaping with a relatively similar frequency. S. mystax is similar to S. midas and S. imperator in the use of supports, but covers greater leaping distances on average, which are nevertheless shorter than those of L. nigrifrons .
We assumed these differences to be reflected in the locomotor morphology, too, and compared various morphological features of the long bones of the limbs. According to our performance and habitat utilization data, we expected the long bone morphology of L. nigrifrons to reflect the largest potential for joint torque generation and stress resistance, because we assume longer leaps on vertical supports to exert larger forces on the bones. For S. mystax , based on our performance data, we expected the potential for torque generation to be intermediate between L. nigrifrons and the other two Saguinus species. Surprisingly, we found S. midas and S. imperator having relatively more robust morphological structures as well as relatively larger muscle in-levers, and thus appearing better adapted to the stresses involved in leaping than the other two.
Conclusion
This study demonstrates the complex ways in which behavioral and morphological ‘levels’ map onto each other, cautioning against oversimplification of ecological profiles when using large interspecific eco-morphological studies to make adaptive evolutionary inferences.
... In sum, these data suggest that, in the evolutionary history of the Callitrichidae, differences in limb proportions and growth ontogeny might have played a major role in shaping ecological and behavioral differences between C. goeldii and L. fuscicollis. These differences include divergence in substrate use (Garber and Pruetz 1995;Heymann and Buchanan-Smith 2000;Berles et al. 2022), niche partitioning, feeding behavior (Bicca-Marques 1999), and positional behavior (Garber andLeigh 2001a, 2001b). It also indicates that limb proportions among callitrichids may be used to distinguish ecologically different taxa. ...
Ontogenetic studies of callitrichid anatomy are limited to research focused mainly on postcranial skeleton of adults. The goal of this study is to compare the ontogeny of postcranial skeletal development in Goeldi’s monkeys (i.e., callimico; Callimico goeldii) with the corresponding data on saddle-back tamarins (Leontocebus fuscicollis). The intermembral, humerofemoral, brachial, crural, and ulna-radius indices of callimicos and saddle-back tamarins were calculated and compared among different age classes in order to assess the implications for their ecology and behavior. Ontogenetic trajectories, including age at growth cessation, were also calculated. It is shown that for a given hindlimb length, L. fuscicollis has longer forelimbs compared to C. goeldii, maintaining this proportion across all age classes. A relatively elongated forelimb observed in L. fuscicollis may have a mechanical role in reducing the force of impact when landing on large vertical substrates. In contrast, hindlimb length and pattern of hindlimb development (such as derived features of the ankle that enhance stability) in callimicos appear to play a critical role in propulsion during trunk-to-trunk leaping. These differences may affect niche partitioning, foraging strategies, and substrate use.
The fibula, despite being traditionally overlooked compared to the femur and the tibia, has recently received attention in primate functional morphology due to its correlation with the degree of arboreality (DOA). Highlighting further fibular features that are associated with arboreal habits would be key to improving palaeobiological inferences in fossil specimens. Here we present the first investigation on the trabecular bone structure of the primate fibula, focusing on the distal epiphysis, across a vast array of species. We collected μCT data on the distal fibula for 21 species of primates, with representatives from most of the orders, and we employed a recently developed approach implemented in the R package ‘indianaBones’ to isolate the entire trabecular bone underlying an epiphysis or articular facet. After extracting both traditional trabecular parameters and novel topological indices, we tested for the posited relationship between trabecular bone and DOA. To disentangle this effect from others related to body size and phylogenetic relationship, we included a body mass proxy as covariate and employed phylogenetic comparative methods. We ran univariate/multivariate and exploratory/inferential statistical analyses. The trabecular structure of the fibular distal epiphysis in primates does not appear to be associated with the DOA. Instead, it is strongly affected by body mass and phylogenetic relationships. Although we identified some minor trends related to human bipedalism, our findings overall discourage, at this stage, the study of distal fibula trabecular bone to infer arboreal behaviors in extinct primates. We further found that body size distribution is strongly related to phylogeny, an issue preventing us from unravelling the influence of the two factors and that we believe can potentially affect future comparative analyses of primates. Overall, our results add to previous evidence of how trabecular traits show variable correlation with locomotor aspects, size and phylogenetic history across the primate skeleton, thus outlining a complex scenario in which a network of interconnected factors affects the morphological evolution of primates. This work may represent a starting point for future studies, for example, focusing on the effect of human bipedalism on distal fibula trabecular bone, or aiming to better understand the effects of body size and phylogenetic history on primate morphological evolution.
Objectives
Despite qualitative observations of wild primates pumping branches before leaping across gaps in the canopy, most studies have suggested that support compliance increases the energetic cost of arboreal leaping, thus limiting leaping performance. In this study, we quantified branch pumping behavior and tree swaying in wild primates to test the hypothesis that these behaviors improve leaping performance.
Materials and Methods
We recorded wild colobine monkeys crossing gaps in the canopy and quantitatively tracked the kinematics of both the monkey and the compliant support during behavioral sequences. We also empirically measured the compliance of a sample of locomotor supports in the monkeys' natural habitat, allowing us to quantify the resonant properties of substrates used during leaping.
Results
Analyses of three recordings show that adult red colobus monkeys ( Piliocolobus tephrosceles ) use branch compliance to their advantage by actively pumping branches before leaping, augmenting their vertical velocity at take‐off. Quantitative modeling of branch resonance periods, based on empirical measurements of support compliance, suggests that monkeys specifically employed branch pumping on relatively thin branches with protracted periods of oscillation. Finally, an additional four recordings show that both red colobus and black and white colobus monkeys ( Colobus guereza ) utilize tree swaying to cross large gaps, augmenting horizontal velocity at take‐off.
Discussion
This deliberate branch manipulation to produce a mechanical effect for stronger propulsion is consistent with the framework of instrumental problem‐solving. To our knowledge, this is the first study of wild primates which quantitatively shows how compliant branches can be used advantageously to augment locomotor performance.