Anthropological Review • Vol. 81(4), 414–422 (2018)

Anthropological Review Available online at: https://content.sciendo.com/anre Journal homepage: www.ptantropologiczne.pl

Analysis of limb movement synchronization in locomotion

Zofia Sikorska-Piwowska1, Piotr Śliwka2, Bogdan Ciszek1

1Department of Descriptive and Clinical Anatomy, Centre of Biostructure Research, Medical University of Warsaw, Poland 2Department of Mathematics and Natural Sciences, Cardinal Stefan Wyszyński University, Warsaw, Poland

Abstract: The authors present an original mathematical model based on features identified with discrete variables using vector and hierarchical cluster analysis in primates locomotion. Proposed model allows to formalize and analyze the synchronization variability of movements in given locomotion types of adaptation and specialization in monkeys, and . The material covers observations of 102 forms including 9 species of primates: the , bonobo, , , gelada, mandrill, brown capuchin and ring–tailed lemur. The studies included also the synchronization of locomotory movements in man. The sequences of moves of pectoral and pelvic limbs, right and left, were studied in four categories: , , and . The locomotion movements depend on the brain centers and allow to find phylogenetic relations between examined forms in the evolution process. The knowledge of the pattern of movements is used in the treatment of paraplegia and paraparesis in humans.

Key words: evolution process of primates bipedality, vector analysis, hierarchical cluster analysis, pattern of movements, treatment of paraplegia and paraparesis.

Introduction The evolution variability of synchro- nization limb movement in terms of lo- The aim of this work is to verify phylo- comotion of primates depends on types genetic relation and contributes to the of their adaptation and specialization explanation of man’s biped posture. As in particular environmental conditions. a tool, the vector analysis and hierarchi- An adaptation type means the state of cal cluster analysis, based on formalized adaptive traits of extremities correlated traits regarding the synchronization of with traits of all organisms. These traits locomotive movements of the ensure an optimal solution of locomo- limbs, were used. tory functions of extremities in the ha- These studies explained the mecha- bitat. Specialization types are selected nism of origin of foot and hand exa- structural functional differentiations of mined by many researches and hadn`t to extremities due among others to inten- be identified in this analysis. sification of given locomotory functions.

Original Research Article Received July 26, 2018 Revised November 13, 2018 Accepted November 15, 2018 DOI: 10.2478/anre-2018-0036 © 2018 Polish Anthropological Society Movement synchronization in primates 415

Transition from to According to these authors, in quadrupedal adaptation is an instructi- evolved to increase the visual horizon as ve example. a strategy against greater predators and Primates belong to the order of mam- competition in savanna-woodland habi- mals. Zoological taxonomy divides this tats. Richmond (2001) assumed that hu- order into two principal groups: Strepsir- man bipedalism originated from arboreal rhini and Haplorrhini. Strepsirrhini are re- quadruped ancestors. Moreover, there presented in our study by lemurs (Lemur were anatomical similarities in the human catta L.) which climb trees with four limbs and baboon hand structures. Carvalho having prehensile hands and feet. Haplor- (2012) claimed that the climate changes rhini are composed of broad nose monkeys reduced forested areas forming selecti- (Platyrrhini) and narrow nose ones (Ca- ve pressure to lead hominine’s ancestors tharrhini). Platyrrhini, like capuchin (Ce- to modify their posture to include a lar- bus capucinus L.), live in South America and ger component of bipedality. Occasional climb from one branch to another hanging bipedality occurs among wild great apes with pectoral extremities. Additionally, linked to food carrying with males trans- some of them use their prehensile tails porting more often than females (Rich- while locomotion. The Catharrhini were mond 2001). Niemnitz (2010) described divided into Cercopithecidae monkeys the evolution of the upright posture and and Hominoidea. The locomotion of the gaits. Oscillatory movements of the limbs Cercopithecidae, like baboons (Papio pa- during locomotion of vertebrates were also pio Desm.) or mandrills (Mandrillus sphinx considered by physicists and mathemati- L.), effects quadrupedally with prehensile cians such as Collins and Steward (1991) hands and feet on branches or on the gro- in terms of their diverse inter-relations. und. Hominoidea like (Hylobates According to Crompton (2008), in the lar L.) and apes like chimpanzee (Pan tro- evolution of the locomotion system from glodytes L.) and bonobo (Pan paniscus L.) the earliest hominids to modern Homo sa- brachiate hanging on branches or step on piens has to be explained how flexed po- the ground quadrupedally (Sikorska-Pi- stures of the hind limb could have prea- wowska et al. 2015). Their pectoral extre- dapted the body for the apes acquisition mities are very elongated in relation to the of straight-legged erect bipedality. Hilde- pelvic ones. brand (1967) analyzed walking and run- In the present paper, the locomotion ning gaits of 26 genera of primates and de- of man was compared with those of scribed typical support sequences of them. monkeys and apes. Human extremities Schmitt (2003) considered that primates evolved in a different way than those of including human showed patterns of lo- other primates, because human pelvic comotion and locomotor control different legs are very elongated in biped loco- from all other . According to this motion, and pectoral ones are shortened. author, hominid bipedalism evolved in ar- In the human hand, the thumb is capable boreal climbing primates. of real opposition to other fingers ena- Type of movement is generated by bling precise movements. the spinal cord centers both for pectoral The evolution of primates locomotion and pelvic limbs. Long-lasting research was examined by Videan and McGrew indicated that they play a significant role (2002) as well as by Williams (2010). in coordinating primates’ locomotion 416 Sikorska-Piwowska, et al. movements (Carvalho et all. 2012; Dietz 2 second one, and so on. If the move- 2002). This knowledge is being used in ments occur at the same time, they are the treatment of paraplegia and parapa- denoted by the same number. The sequ- resis in humans - victims of spinal cord ence allows to estimate the differences or injuries. This research is focused on acti- similarities between the studied forms vation of peripheric spinal neurons coor- in the types of movements. For exam- dinating pelvic limbs activities. This can ple, in walking moves of the chimp, the be done by spinal cord stimulation or right chest limb (RC}, which is the first by modification of rehab programs and to move is numbered 1, next moves the the usage of limbs’ exoskeletons (van left pelvic limb (LP) that is numbered 2, den Brand et al. 2015). These categories after that moves the left chest limb (LC) are the measure of brain evolution and numbered 3 and finally the right pelvic allow to find phylogenetic relations be- limb (RP) numbered 4. So its sequence tween examined forms. Particular limb of movements was represented in Table movement patterns are supposed to be 1 denoted by (3,1,2,4). There is also 0 in invariable within the populations stu- the table which indicates the lack of the died which are considered to be inde- type of movement. pendent forms. In the rows of the table there are gro- ups of stages of the movement tabula- Material and methods ted. The 16 stages are divided between all types of movement as walking, run- Observations were carried out in the ning, jumping and brachiation. This way, Sanctuary in the Swe- every species is described by 16 stages etwaters Game Reserve in Kenya, in the of movements which compose a vector

Orangutans Sanctuary in Sumatra and xi={xi1, ..., xiN} determining a location of Tsaratanana Strict Nature Reserve in Ma- a given species in a multi-dimensional dagascar. This research was complemen- vector space with information about their ted in zoos in Warsaw and Gdansk. synchronization (N=4 or N=16). Eight species of primates were ob- These 16 stages of movements divi- served at the following numbers: ring-ta- ded into 4 types of movements: walking iled lemur (14), tufted capuchin monkey - W, running - R, jumping - J and brachia- (14), baboon (14), mandrill (14), gibbon tion – B were considered to be discrete (10), orangutan (12), chimpanzee (12) characteristics which characterize each of and bonobo (12). In total information the primate forms. These vectors genera- about 102 specimens was collected. The te matrix X (dim: 9x4 or 9x16) observed results were analyzed. X = {x1, ..., xQ} Table 1 presents four types of move- consists of movement stages vectors ments considered: walking, running, jum- for all species (i∈Q, Q = 9 - number of ping and brachiation with information on species of monkeys and human). the left and right chest and pelvic limb The lack of a particular type of move- synchronization for all analyzed prima- ment in the examined species was custo- tes, including man. This synchronization marily designated by the value of 0. As was indicated by the sequence of the mo- an example the lack of brachiation occurs vements represented by numbers from both in humans and in the mandrill and 1–4 where 1 denotes the first movement, baboon. Movement synchronization in primates 417

Table 1. Synchronization order of the limbs movement for the examined primates Limbs Walking Running Jumping Brachiation Forms LC RC LP RP LC RC LP RP LC RC LP RP LC RC LP RP L 1 3 4 2 1 3 4 2 2 2 1 1 1 3 2 4 CM 3 1 2 4 3 1 2 4 2 2 1 1 2 1 3 4 BA 2 4 3 1 4 2 3 1 2 2 1 1 0 0 0 0 MN 2 4 3 1 4 2 3 1 0 0 0 0 0 0 0 0 G 0 0 1 2 0 0 0 0 3 2 1 1 2 1 0 0 O 3 1 2 4 3 1 2 4 2 3 1 1 2 1 3 4 CH 3 1 2 4 3 1 2 4 2 3 1 1 2 1 3 4 BO 3 1 2 4 0 0 1 2 0 0 0 0 2 1 3 4 M 1 2 2 1 1 2 2 1 1 2 2 1 0 0 0 0 𝑁𝑁 Legend: Limbs: LC-left chest, RC-right chest, LP-left pelvien, RP-right pelvien. Forms: Lemur6 (L), Capuchin (CM), Baboon2 𝑒𝑒𝑒𝑒𝑒𝑒 2 𝑖𝑖𝑖𝑖 𝑗𝑗𝑗𝑗 (BA), Mandrill (MN), Gibbon (G), Orangutan (O), Chimpanzee (CH),𝜌𝜌 Bonobo= 1 −(BO), Man (M). Number∑(𝑅𝑅 from− 𝑅𝑅 1 to) 4 represent the order of movements, 0 – lack of movement. Source: own calculations. 𝑁𝑁(𝑁𝑁 − 1) 𝑘𝑘=1

Preliminary analysis of all phases and sters was estimated, types of movements was done by means of Spearman`s rank correlation coeffi- N cient ρ in the form: 𝑁𝑁 2 xixj ik jk d = √∑6k=1(x − x ) 2 𝑁𝑁 where:𝜌𝜌𝑒𝑒𝑒𝑒𝑒𝑒 d = –1 −Euclidean2 distance∑(𝑅𝑅𝑖𝑖𝑖𝑖 between− 𝑅𝑅𝑗𝑗𝑗𝑗) 2 xixj 𝑁𝑁(𝑁𝑁 − 1) 𝑘𝑘=1 𝑒𝑒𝑒𝑒𝑒𝑒 6 𝑖𝑖𝑖𝑖 𝑗𝑗𝑗𝑗 pairs of species x and x for each limb, 𝜌𝜌 = 1 − 2 ∑(𝑅𝑅 − 𝑅𝑅 ) i j where: R , R is𝑁𝑁 (rank,𝑁𝑁 − 1k) is𝑘𝑘= index1 descri- k-index describing the type of limb in a ik jk m 2 ∈ bing the type of limb in given stages and given phase and type of motion,i i,j Q, types of movement , i,j∈Q, ESS = ∑i= 1(x − x̅) but ρ only shows correlations be- - second, a pair of clusters was selected N tween pairs of species and they do not al- that, after the merging approach 2the fo- dxixj = √∑ m (xik − xjk) low unique grouping Nof species with2 phy- cus of the minimumk =differentiation1 by m i logenetic relationships.xixj Forik thisjk purpose, the ESS (errorT sum= ∑ of i=squares):1Var(C ) d = √∑k=1(x − x ) a hierarchical cluster analysis with the agglomeration method (merging smal- m 2 ler clusters into larger clusters) and the i m ESS = ∑i=1(x − x̅) Ward measure of the inequality2 between where: m is the number of species (m=1 i clusters wereESS applied= ∑i = (Murtagh1(x − x̅) and Le- to m=9). gendre 2014). The classic “elbowm method” (also known as the “scree plot”, Thorndi- Tm = ∑ Var(Ci) Two steps were done: m ke 1953) is used to iselect=1 the number m i - first, the EuclideanT = ∑i =distance1Var(C ) between of clusters based on the rule: find such clusters that uses the variance analysis Var(C1)+…+ Var(Cm) that adding a new approach to minimize the sum of the cluster Cm+1 with new variance Var(Cm+1) squares of the deviations within the clu- does not significantly changes the sum 𝑁𝑁 6 2 𝜌𝜌𝑒𝑒𝑒𝑒𝑒𝑒 = 1 − 2 ∑(𝑅𝑅𝑖𝑖𝑖𝑖 − 𝑅𝑅𝑗𝑗𝑗𝑗) 𝑁𝑁(𝑁𝑁 − 1) 𝑘𝑘=1

418 N 2Sikorska-Piwowska, et al. dxixj = √∑ (xik − xjk) k= 1 (Σi=1,..,m Var(Ci) / Σi=1,..,m+1 Var(Ci)≈1). boon is similar to the of In the graph with the increase in the the lemur, which is a primordial form of number of clusters onm the abscissa, we the primates, whereas the gibbon and the observed on the ordinates a “gentle2 de- man diverge from the others. Gibbons ESS = ∑ (xi − x̅) scent” of the sum of variancei= 1 walk on two limbs keeping their balance with their arms outstretched, and man

m uses the upper limbs as pendulums mo- m i ving in the rhythm of the lower limbs. T = ∑i=1Var(C ) where: Tm - index of the number of clu- In the type of running locomotion four sters, Ci – i-th cluster, Var (Ci) - value of groups were formed. The order of move- variance within the i-th cluster, m - opti- ment of the limbs resembles the previous mal number of clusters. type; however, bonobos and gibbons are

Based on the Tm index and the type of distinguished from the others and form a movement, homogeneous groups were common group, while the rest of apes are identified that best describe the phylo- similar. Lemur as a primary form is lin- genetic relationships between species. In ked, on the one hand, to mandrill and ba- the next step each type of movement was boon, and on the other hand, with man. analysed. In the type of jumping locomotion, two groups were formed. Bonobo and Results mandrill jump similarly. The orangutan, chimpanzee, gibbon, baboon, capuchin Two types of analysis were done: first, and lemur form one group, while man detection of the numbers of clusters, and jumps in his own way. This dendrogram second, dendrograms of the connection points out to the uniformity of the arbo- between the examined forms based on real quadruped adaptation of the lower separate types of movements such as wal- limbs of all examined primates, except king, running, jumping and brachiation for man who represents the type of bipe- and all types of movements together. The dal adaptation. visualization of the number of clusters In the type of brachiation two gro- (vertical line on graphs) and dendro- ups were formed. Brachiators, like the grams on Figures 1 and 2 were presented apes and capuchins, come from primitive (the species name abbreviations identical forms represented by lemur, thus forming as those in Table 1). the same group. The second one con- In the type of walking locomotion four sisted of humans, baboons, mandrills and groups were formed. Apes, represented gibbons. Human pectoral limbs have lost by the chimpanzee, orangutan and bo- their locomotion function but retained nobo (Catarrhini), and the capuchin as a the features of the primordial arbority, representative of the broad nose monkeys which allows to link humans to the babo- (Platyrrhini) in the dendrogram, formed on and the mandrill. The gibbon, which is one group, because their pelvic limbs, a type of brachiator different than the which are used to walk on the ground, and capuchin due to the well-developed have a similar form as that of the quadru- thumb and occasional bipedalism, is also pedal apes, but unlike them, they knuc- assigned to this group. kle-walk on the elongated chest limbs. In the case of all type of movements, Quadrupedalism of the mandrill and ba- five groups were formed. Lemur is in the Movement synchronization in primates 419 initial position for all examined forms. man’s bipedalism was a type of quadru- Apes form one group with capuchin ex- pedal primitive adaptation for climbing, cept for the gibbon, whose locomotion which is characteristic for the mandrill developed in a different direction than and baboon. Bonobo is a separate case, that of the others. Proof of this is its han- incorrectly considered to be the closest d-built construction with a fully develo- form to a human being. ped thumb, which allows for acrobatics while hanging on the branches. Other Discussion brachiators have a reduced thumb. Man specialized in bipedalism as illustrated Locomotive adaptation types, such as by the extension of the lower limbs, as primitive climbing, primitive hanging opposed to brachiators with lower limbs (brachiation) and human bipedness pre- shorter than the upper ones. However, dispose the ways of limb movement syn-

Fig. 1 Dendrograms of the numbers of clusters of examined species in defined types of movements in the locomotion. Source: own calculations. 420 Sikorska-Piwowska, et al. chronization in walking, running, jum- In the group of monkeys and apes the ping and brachiation. Adaptations types most distant connections are related to were described by Sikorska-Piwowska the gibbon. Cooper (1999) confirmed gi- (1984). bbon`s distinct specialization in the lo- Lemurs, considered as a primary gro- comotor movement. It allows to assume up of primates (Hofstetter 2002; Kay et that gibbon`s evolution line has separa- all. 1997; Ross et all. 1998), have been ted from the other examined species. added to the examined species. We can During locomotion the chimpanzee, assume that this group forms a pluripo- orangutan and capuchin monkey have a tential variety which are linked in each similar movements synchronization. One quadrupedalism to mandrill and baboon can assume that this is the result of a on the one hand and to man on the other parallel evolution of apes and broad-no- hand. sed monkeys that took place on the two

Fig. 2 Dendrograms of multilateral connections between the groups of examined species in defined types of movements in the locomotion (abbreviations identical to those in Table 1). Source: own calculations. Movement synchronization in primates 421 continents separated from each other - Conclusions Africa and Asia - formed from the former Pangea (Fleagle 2013). This similarity of Our study on primates’ locomotion created locomotion between these two groups a new algorithm which allows us to defi- was already noticed by Sikorska-Piwow- ne the movement patterns for examined ska (1974) in her work concerning the species. The obtained results allow better ossification order of bases. understanding multidimensional relations Moreover, it is perhaps the plane of the between examined traits of the primate lo- moves or the centre of gravity which de- comotor apparatus. This study may be used termines this. to verify phylogenetic relation and contri- The bonobo is a species which is cle- butes to the explanation of man’s biped arly separated from both apes and man. posture, as well as in the treatment of para- Perhaps this species has started a new plegia and paraparesis in humans by modi- locomotive tendency. This is in oppo- fication of rehab programs and the usage of sition to Videan`s work (2002). limbs’ exoskeletons. Man, in the course of his phyloge- netic development, has also gone thro- Authors’ contributions ugh the process of leaving the life in trees (Osborn and Homberger 2015), ZS-P conceived a paper, provided mate- which is currently marked in his move- rial for analysis, interpreted results, wro- ment synchronization characteristic of te draft manuscript, PS performed stati- baboons in all movement types possible stical analyses and interpreted results, for these species (with the exception of BC discussed study results. All authors brachiation, Vallois 1956). Relict feature have read and approved the final version of this relation is the possibility of full of the manuscript. opposition of the thumb to the other fin- gers observed in the baboon. These facts Conflict of interest may suggest that movement patterns present in earlier evolution stages of pri- The authors have no conflicts of interest mates could be introduced to rehabilita- to declare. tion programs (especially for incomple- te damages like para and tetraparesis). Corresponding author Also modification of rehabilitation pro- grams in ischemic strokes with half-de- Zofia Sikorska-Piwowska, Department ficit could take into account locomotive of Descriptive and Clinical Anatomy, evolution of primates. Centre of Biostructure Research, Medical The forms studied represent the apex University of Warsaw, Chałubińskiego 5, of the phylogenetic tree cut by the pla- 02-004 Warsaw, Poland ne of the present times. Evolutionary E-mail: [email protected] connections between them based on locomotive movement synchronization References could be evidence of their similarity on van den Brand R, Mignardot JB, von Zitze- the one hand and diversity in their ada- witz, J, Le Goff C, Fumeaux N, Wagner F, et ptation and specialization on the other all. 2015. Neuroprosthetic technologies to hand. augment the impact of neurorehabilitation 422 Sikorska-Piwowska, et al.

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