Morphometry of the Femur, Tibia and Fibula of Plecturocebus caquetensis

The Colombian Amazon primate, Plecturocebus caquetensis, is a species that belongs to the Pitheciidae family (Carneiro et al., 2016). This family is from Cauca and Caquetá departments in Colombia (Villota et al., 2021). Besides, it has limited space distribution (Suarez Ramirez​ et al., 2021) in municipalities such as Piamonte, Solano, Solita, Valparaíso, Curillo, San José del Fragua, Milánand Albania (Defler et al., 2016). Following this idea, this species was only reported until 2010 (Defler, 2014) because, during the early years, public order difficulties in the region did not allow investigators’ entrance (Defler and Garcia, 2016). However, this species has been studied recently considering some aspects of its natural history (Van Roosmalen ​et al., 2002) in which travel habits are mentioned to define the species as a jumping primate (Rocha et al., 2019) considering the species’ size (Byrne et al., 2016) and anatomical design (Isidro, 1994) that define the species as qualified for its habitat (Osbahr et al., 2009). Nonetheless, this information is general. That is why the investigations’ developments are required to recognize the anatomical, morphometrics and functional conditions that define the species’ecology (Garcia and Defler, 2011).
       
The aforementioned aspects are considered by other authors from areas such as biology (Garcia and Defler, 2013), trophic ecology (Defler et al., 2016), conservation (Defler and Garcia, 2016) and phylogenetics (Boubli et al., 2019), but thorough findings related to size and function of a specimen’s anatomical structures, as input to understand populations’ necessities (Garcia et al., 2010) that define handling and health conditions (Lucy et al., 2018).
       
The Plecturocebus caquetensis anatomy has been only tackled from the descriptive point of view of its osteology (Montilla-Rodriguez et al., 2023), but morphometrics or functional data are unknown because in 2010 the principal studies focused on distribution (Villota et al., 2021), endemism (Defler et al., 2016) and population size (Acero-Murcia et al., 2018) affected by deforestation for cattle raising (Lacetera, 2019), illegal mining, illicit cropsand oil exploitation (Lizcano et al., 2021).
       
Thus, this study externalizes morphometric data that contribute to this type of knowledge, selecting appendicular skeleton structures such as the femur, fibula and tibia, that are important for locomotion in the habitat  (Ariana et al., 2020). In this sense, relating obtained values to functional aspects (LLeo, 2015) works as a contribution to veterinarian knowledge (Bharti et al., 2022) of the species to understand related conditionals to the locomotion, the jump (Fleagle et al., 2016) and mechanical loads  (Morimoto, 2012) that the species has to endure in its habitat.

It utilized bone structures from primates of the Plecturocebus caquetensis species, preserved at the Instituto de Ciencias Naturales of Universidad de Colombia and the Museo de Historia Natural of Universidad de la Amazonia. These bone structures were used to study their anatomy (Sepkoski, 2009) by using essentially existent corpses, without attacking specimens that still exist in the natural environment. Besides, striving to prevent its extinction (Monsalve-Buritica, 2019) was important because the species population does not exceed 250 individuals (Garcia and Defler, 2011). The code of ethics for Veterinary Medicine, Veterinary Medicine Zootechnics and Zootechnics in Colombia (Ley 576, 2000) as well as the Sentence C-666 (2010) from the Corte Constitucional, the Ley 84 (1989), Ley 1774 (2016) and the articles 8 and 79 from the Constitucion Política de Colombia (1991) establish the ban on ending wildlife in honor of science.
       
Therefore, from the existent bone structures in the biological collections the femur, tibia and fibula were considered. In this sense, these bones were measured by using a digital vernier (Gualda-Barros et al., 2012) with 0.01mm precision (Kohn and Lubach, 2018) considering different studies on this topic (Ciochon and Corruccini, 1975). In this order of ideas, to carry out the morphometric registration, variables corresponding to articular surfaces were mainly registered, providing information about the primate’s mechanics of movement in other parts of the bone (Ruff, 2002). This is because there is a close congruence between neighboring structures and the interdependence of all the functional components of the joints (Vancata, 1991). In the same line of thought, bone structure images were taken by using the digital camera CANON® EOS Rebel T3 to locate the points of reference of the obtained variables (Fig 1 and 2). 




       
Initially, the femur was addressed considering the proposed variables by (Ciochon and Corruccini, 1975), Fleagle and Meldrum (1988), Elissamburu (2004) and Blanco-Rodriguez et al. (2015) to register the following data (Table 1).


       
Subsequently, it was obtained data about the variables in the structures corresponding to the tibia and fibula according to Fleagle and Meldrum (1988), Aiello and Dean (1996) and Blanco-Rodriguez et al. (2015) are registered below (Table 2).


       
In this sense, the obtained values were useful to generate summary measures such as mean and standard deviation. This was carried out by using the Infostat® software considering the obtained data about the structures of the right and left pelvic limbs of the specimens. Moreover, it was sought to demonstrate the general distribution of the data for each of the variables to locate those that present greater variance.

In Table 3, significant differences are apparent in all variables between the left and right Femur, Tibia and Fibula, with the right side showing greater development in all cases. Additionally, LT exhibits a higher standard deviation compared to the other variables, followed by LBT, LE, LF, LM1, LM2 and LD, in that order (Table 3).


       
In Fig 3, it can be observed that LT and LBT are the variables that present the highest coefficients of variation and both are related to the tibia, given that the biceps femoris, semitendinosus, vastus lateralis, gastrocnemius and popliteus muscles have their origin or insertion in spaces determined by these variables (Polly, 2007) and their joint functioning determines the close relationship that exists between them. On the other hand, the variables LE, LF, LM2, LM1 and LD, are associated with the femur and the fibula, presenting a certain relationship between them, based on their variations in size and function (Ankel-Simons, 2007), since the adaptation of the axis (Fig 1) allows bending in multiple directions in order to reduce the harmful consequences of a new mechanics and this determines the locomotor behaviors of primates and the positional behaviors (Carlson, 2005).


       
Likewise, the muscles that are inserted in the proximal end of the femur allow to extension of the limb by turning it around the head (Polly, 2007), in such a way that the muscles that are related to the body of the femur and the axis, indistinctly determine the conditions of the variables. The diaphysis, for its part, functions as an engineering beam, providing limb stiffness, particularly against bending and torsional loads (Argot, 2002), allowing the femur to resist bending loads in the caudolateral/craniomedial direction and allowing the bone to act as an energy absorber when running or jumping in a pronograde position. This makes the geometric construction of the femur ideally suited to resist high bending loads below the femoral diaphysis, particularly in the mediolateral plane (Sargis, 2002).
       
The LBT and LF variables, along with their standard deviations, should be highlighted as they meet the two previous conditions between the tibia and fibula. The length of the tibia depends on the activity carried out by the muscles, with only a small percentage of this load being supported by the fibula (Funk et al., 2004). This explains why the fibula’s length and diameter are always smaller. As the longest and widest bone in the leg region, the tibia is responsible for weight bearing in primates such as Plecturocebus caquetensis. It is connected by two slightly mobile joints (synovial joints) at the proximal and distal ends (Ankel-Simons, 2007). In arboreal primates where jumping is part of locomotion, the proximal end of the tibial shaft is more mediolaterally compressed (Fleagle and Meldrum, 1988). The insertion of the quadriceps femoris muscle determines speed and agility by allowing rapid extension of the knee (Salton and Sargis, 2009; Ruff and Runestad, 1992; Szalay and Sargis, 2001).
       
The length of the fibula affects the agility and range of movement of the lower limb required for quadrupedal arboreal locomotion (Marchi, 2007). It is mobile due to the characteristics of the proximal and distal tibiofibular joints, which have adapted to perform rapid and sudden movements (Barnett and Napier, 1953; Salton and Sargis, 2009). However, the fibula’s low robustness in comparison to the tibia is because of its position and its relatively minor role in bearing mechanical loads (Marchi, 2007).
   
The other variables obtained from the femur, tibia and fibula of P. caquetensis, with coefficients of variation less than one, do not show significant differences between them. This is because there is a total synergy between structures and joints for the transmission of force (Marchi, 2007) associated with all these variables. For example, the variable LC reflects a mechanical adaptation to resist flexion forces during jumping (Ford, 1990) and the variables LTM, LTMa, Lca/T, ATM and ATMa are related to the vastus lateralis and quadriceps femoris muscles, which are also linked to knee extension associated with jumping (Salton and Sargis, 2009).
       
It is important to note that the differences between the right and left bone structures in all cases determine specific aspects of movement asymmetry. While there are no recognized references to this in primates, it is indicated in humans that high impacts and constant bone tension can lead to size gain (Nikander et al., 2010). Given that Plecturocebus caquetensis is a primate that jumps and moves on small tree branches, its posture may reflect this. However, detailed studies in its natural habitat, similar to those carried out by Cubi and Llorente (2021) or in the past by Colell (1992) focusing on the hind limbs, are necessary to identify the reason for this preferred posture.

The longitudinal variables of the femur, Tibia and fibula show a greater variation due to the effect of the muscles that are inserted in them, an aspect that may be associated with physical factors of the environment related to the architecture of the forest and particularities of the primate such as age, sexand hierarchical level.
       
Understanding morphometry provides information on some functional aspects that determine the well-being of primates, facilitating the discernment of characteristics necessary for confinement areas or habitat conservation conditions.

This study was supported by the University of the Amazon, under the direction of Dr. Fabio Buriticá Bermeo.
 
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The views and conclusions expressed in this article are solely those of the authors and do not necessarily represent the views of their affiliated institutions. The authors are responsible for the accuracy and completeness of the information provided, but do not accept any liability for any direct or indirect losses resulting from the use of this content.
 
Informed consent
 
Permits related to animal handling were not required for this study, since the work involved anatomical structures stored in biological collections.

The authors declare that there are no conflicts of interest regarding the publication of this article. No funding or sponsorship influenced the design of the study, data collection, analysis, decision to publish, or preparation of the manuscript.