Article pp.111-120 du Vol.26 n°3-4 (2014)

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NOTE /NOTE

Bipedalism in non-human primates: a comparative review of behavioural and experimental explorations on catarrhines

Bipédie chez les primates non humains. Bilan croisé des recherches comportementales et expérimentales sur les catarrhiniens

F. Druelle · G. Berillon

Received: 7 February 2014; Accepted: 11 March 2014

Abstract Non-human primates are commonly used as comparative models to investigate the evolutionary origins of habitual bipedal walking. After almost a century of research in the field of behaviour and functional anatomy, the need for integrative analyses is being widely discussed.

In that perspective, the purpose of this note is to report on the available literature on quantitative behavioural and experimental studies of bipedalism in catarrhines. Examples are given of their respective contributions to fundamental knowledge on bipedalism in non-human primates. We then introduce various prospects for integrative explorations with a view to developing evolutionary hypotheses and to improve existing fundamental knowledge through experi- mental studies of the bipedal walking function in its ecologi- cal and behavioural contexts.

Keywords Bipedalism · Positional repertoire · Experimental analyses · Catarrhini · Evolution

Résumé Les primates non humains sont couramment utilisés comme modèles comparatifs pour investiguer les origines évolutives de la marche bipède habituelle. Après presque un siècle de recherche dans le domaine du comportement et de l ’ anatomie fonctionnelle, une vaste réflexion sur la nécessité de l ’ analyse intégrative est engagée. Dans cette perspective, la présente note propose un rapport de la littérature disponible concernant les études quantitatives comportementales et expérimentales de la bipédie chez les catarrhiniens. Quelques exemples illustrent leur contribution respective à la connais-

sance fondamentale de la bipédie chez les primates non humains. Des perspectives d ’ explorations intégratives sont données, pour l ’ élaboration d ’ hypothèses évolutives, ainsi que pour améliorer cette connaissance fondamentale par l ’ étude expérimentale de la marche bipède replacée dans son contexte à la fois écologique et comportemental.

Mots clés Bipédie · Répertoire positionnel · Analyses expérimentales · Catarrhini · Évolution

Introduction

Non-human primates (NHP) have been commonly used for almost a century as comparative models to investigate the evolutionary origins of habitual bipedal walking. One reason is that they can be considered, in several respects, as repre- sentative of potential functional precursors of habitual biped- alism (see e.g. [1] for a recent review). Moreover, during the last 50 years, field-based studies of the positional repertoire of primates have demonstrated that bipedalism is common among catarrhines [2,3], the closest relatives to humans, as well as in other primates [4,5], which raises the question of the anatomical and biomechanical foundations of this partic- ular behaviour. This question has been addressed in compar- ative and functional anatomical studies (see e.g. [6] for a synthesis and [7] on experimental explorations). The litera- ture in the fields of behaviour and functional anatomy is abundant and varied. After almost a century of field and laboratory-based explorations, the use of NHP models to further our understanding of the evolutionary origins of habitual bipedalism in the most integrative

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manner possible (see e.g. [8]) is being widely discussed.

F. Druelle

Functional Morphology Laboratory, Department of Biology, University of Antwerp, Universiteitsplein 1, B-2610 Antwerpen, Belgium

F. Druelle · G. Berillon (*)

UPR 2147 CNRS, 44 rue de l’Amiral Mouchez, Paris, France e-mail : [email protected]

1An integrative approach combines several approaches of a single individual or sample; in this case, the ideal integrative approach would combine behavioural, anatomical and biomechanical explorations.

DOI 10.1007/s13219-014-0105-2

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a comparative review of original quantitative behavioural and experimental studies on bipedalism in living non- human catarrhines. We have restricted our note to these taxa because, as they are phylogenetically closest to humans, they are likely to be more informative than other primates on the nature of bipedalism and what it could represent in the positional behaviour of hominin ancestors. We provide examples of the contributions of behavioural and experimen- tal studies to fundamental knowledge on bipedal locomotion in primates, and then briefly report on prospects for integra- tive explorations.

Quantitative behavioural studies of bipedalism

In many catarrhine species, bipedal behaviour patterns repre- sent clearly identified modes in the positional repertoire (loco- motion and posture) [9]. Table 1 provides a list, which seeks to be as exhaustive as possible, of the species for which bipedal behaviour patterns have been quantified, with the cor- responding studies (for a review of previous qualitative stud- ies see [2]). The table shows that bipedal behaviour patterns have been identified in each family and sub-family, and that hominoids have received more attention due to their phyloge- netic closeness to humans. The great majority of the species were observed in their natural environment, with data pro- vided on the ecological correlates of their positional reper- toires, some focusing on ontogeny, seasonality, body size effect, etc. (for a theoretical framework see [10]). However, analyses of captive animals also provide original and addi- tional information, including more precise individual data (e.g. age, body mass and individual variations).

Studies of the positional repertoire show that (1) bipedal- ism is spontaneously performed in different ways i.e. assisted and/or unassisted, moving and/or standing, in shuffling, and in arboreal and/or terrestrial contexts (see e.g. [11]). (2) The bipedal behaviour is generally infrequent (<15%)

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; for exam- ple, in adults, lowland gorillas have the highest percentage of bipedal walking in an arboreal context, at 13.7% (recalculated by Hunt, see Table 10.8 [12]), while the lowest frequencies of bipedal walking are usually observed in cercopithecines and colobines, e.g. <1% in Colobus (see Table 6 in [13]).

(3) Bipedalism is more frequent in infants than in adults (e.g. 6% versus 1.8% respectively for bipedal walking in Pan, [14] and 1.73% versus 0% respectively in Papio [15]) (see also [2,16-18]).

Although few studies have focused on bipedalism, they nevertheless show that it is commonly observed when ani-

food patches and transporting food items (see also [2,11,19- 21]), but also when avoiding predators [2,11,22] and in social contexts such as playing (mainly during infancy), in displays of dominance or friendly contacts, in stereotyped copulation postures in males [2,11], in sequence with other locomotor modes, and finally, in particular contexts such as orientation [2]. Bipedalism has also been correlated with specific ecological contexts such as moving on flexible branches [11,23] and in waterlogged environments (flooded forests, swamps, etc) (for a review see Table 1 in [24]).

Finally, when the environment is set up experimentally, the frequency of bipedal behaviour increases significantly [25].

Achieving bipedalism is therefore seen as context- dependent, but may also be greatly facilitated when it is assisted, for example by branches or foliage when animals are observed moving through trees (see e.g. [21,22]).

Experimental studies of bipedal gaits

Experimental studies of bipedal gaits in catarrhines address the following question: what, anatomically and biomechanically, enables non human catarrhines to stand and walk bipedally?

Schmitt [7,26] provides a representative review of experimen- tal analyses of various locomotor modes, including bipedal- ism, in non-human primates. In this vein, table 1 provides an exhaustive list of original studies on bipedal gaits in catarrhines that were conducted from the evolutionary perspective

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.

Since the very early descriptive analysis of bipedal walk- ing in a juvenile chimpanzee by Elftman and Manter, this field of research has mainly expanded through laboratory- based experiments; today, studies are often designed as inte- grative experiments

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. Data are available for almost all fami- lies and subfamilies of catarrhines, except colobines. Due to the sometimes restricted access to the primates as well as to experimental constraints, the data are very fragmented: for some species (e.g. Macaca fuscata), all biomechanics aspects are well documented, but very little in others (e.g.

Gorilla gorilla), and the samples studied usually consist of a few individuals of varied ages. Despite these inherent lim- itations in experimental research on NHP, and although their representativeness with regard to natural biological varia- tions can be questioned, fundamental comparative biome- chanics data are now available for non human bipedal (ter- restrial) locomotion, especially in Pan paniscus, Pan troglodytes, Hylobates lar, Macaca fuscata and Papio

2The frequencies published depend on whether locomotor and postural repertoires, on the one hand, and arboreal and terrestrial contexts on the other hand, are considered in combination or not.

3Several neurological contributions provide data on the biomechanics of bipedal walking in Macaca fuscata and M. fascicularis (see e.g. [27,28]).

4Integrative biomechanical experiments tend to combine kinematic, kinetic and morphological investigations of a single sample.

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Table1SummaryofbehaviouralandexperimentalstudiesonbipedalisminCatarrhini/Synthèsedesétudescomportementalesetexpérimentalesdelabipédie chezlescatarrhiniens. BEHAVIOURALSTUDIESEXPERIMENTALSTUDIES SpeciesSample size StudysiteSex/AgeclassDataBipedal component Reference(s)Sample size

StudysiteSex/AgeclassDataReference(s) Hominoidae Hominidae Pantroglodytes33/70Wild/habM&F/InftoAdL,HX[17,18]2Lab-TM/Juv-AdT,K[30] idemM&F/AdL,Po,H,ActX[31,32]1Lab?K,P[33] 26Wild/hab11M&15F/AdL,Po,H,ActX[34,35]1Lab?T,K[36] idemB,H,ActX[11]2Lab?K[37] 53/160Wild/hab32M&21F/InftoAdL,PoX[14]1Lab-UM/JuvEMG[38,39] 11Wild/habM&F/AdB,ExpX[19]1Lab-TF/SubadT,K,F,EMG[40] 10Capt5M&5F/AdBX[41]idemT,F[42-44] 14Capt8M&6F/InftoAdB,Act,ExpX[25,45]1Lab-TM/SubadK[46-49] 10/20Wild/phabM&F/Inf-AdB,H,ActX[50]4Lab-U1F&3M/JuvEMG[51] 13idemM&F/InftoAdB,H,ActX[21]1Lab-T1F/JuvT,K,F,EMG[52] 1Lab-T?/AdT,K[53] 1Lab-UM/AdEMG[54,55] 1Lab-TF/JuvEMG[56] 5Lab-T2F/Ad;1M&2F/Inf-AdT,F[57] idemT,K[58,59] 1Lab-U?T,K,F[60] 5Lab-T2M&3F/Juv-AdT,K,F,E[61,62] Panpaniscus?Wild/phabM&F/InftoAdL,arborealX[17]5Encl-U4M&1F/Inf-Juv-AdT[63] ?Wild/phabM&F/AdL,Po,H,ActX[31]idem4M&1F/Inf-Juv-AdT,K,F,P[64,65] ≈65Wild/hab orphab

M&F/?Po,feeding/ arboreal

[66]idem4M&1F/Inf-Juv-AdK[67] ?Wild/unhab?/?L,arborealX[3]idemM&F/Inf-Juv-AdK,F[68] ?Wild/unhab?/?L,arborealX[69]idem2M&2F/AdT,K,P[70] 14Capt8M&6F/InftoAdB,ActX[25,45]idem1M&1F/AdT,P[71] Gorillagorilla11Wild/habM&F/Juv-AdL,Po,H,ActX[72]1Lab-UF/JuvEMG[38,39,73] 37/51Wild/habM&F/InftoAdL,HX[18]1Capt?P[74] ?Wild/phabM&F/?L,Po,HX[75] ?/14+?Wild/phabM&F/AdL,Po,H,ActX[76,77] Pongopygmaeus2Wild/habM&F/AdL,Po,travel[78]1Lab-UF/SubadEMG[38,39] 8Wild/hab2M&6F/JuvtoAdL,Po,H,Act[79]1Lab-UM/JuvEMG[51] 2Wild/hab2F/AdL,Po,H,ActX[80]1Lab-TF/AdT,F[44] ≥4Wild/hab1M&≥3F/AdL,Po,H,feedX[81]1Lab-TM/AdEMG[55] 10Wild/hab6M&4F/JuvtoAdL,Po,H,ActX[22,82]1Capt?F,P[1] (Suitepagesuivante)

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Table1(suite) BEHAVIOURALSTUDIESEXPERIMENTALSTUDIES SpeciesSample size StudysiteSex/AgeclassDataBipedal component Reference(s)Sample size

StudysiteSex/AgeclassDataReference(s idemB,HX[23]1Capt?T,K[74] 2Capt1M&1F/AdL,PoX[83] 13Wild/hab6M&7F/InftoAdPo,H,feedX[84] 22Wild/hab15M&7F/JuvtoAdL,Po,H,ActX[85] Hylobatidae Hylobateslar?Wild/??/AdL,H,ActX[86,87]1Lab-F/SubAdT,K[88] 1Lab-TM/AdT,K[30] 1Lab-TF/JuvEMG[89] 2Lab-UM&F/AdEMG[51] 2Lab-UM&F/AdEMG[54] 2Lab-TM&F/JuvEMG[56] 6Encl-U1F&2M/Ad;1M/InfT,P,F[90] idem1F&2M/Ad;1M/JuvT,K[91] idem1F&2M/Ad;1M/Juv; 1F/Inf

T[92] idem1F&2M/Ad;1M/JuvT,K,F[93] idem1F&2M/AdT,F[94] Hylobatesagilis2/4Wild/habM&F/AdL,H,travelX[95]1Lab-TM/JuvEMG[89] 3/4Wild/hab2M&1F/Juv-AdL,Po,H,ActX[96]1Lab-TM/AdK[97] 1Lab-TF/JuvT,K,F,EMG[40] idemT,F[42-44] 1Lab-TM/JuvT,F,EMG[98,99] 1Lab-T?/AdT,K(No)[53] Hylobatespileatus6Wild/hab2M&4F/InftoAdL,Po,H,ActX[100]afamilyEncl-U?K[101] Hylobatessyndactilus?Wild/??/AdL,Po,H,ActX[86,87] Cercopithecoidae Cercopithecidae Cercopithecinae Macacafuscata16Wild/hab5M&11F/AdL,Po,H,ActX[102]3Lab-T1F&2M/AdT,K,F,EMG[40] idemT,F[42-44] 1Lab-T1F/JuvT,K,F,EMG[52] 2Lab-T?/AdT,K[53] 2Lab-TM&F/SubAdEMG[56] 3Lab-TM/AdT,K[103,104] 7Lab-5T/2UM/AdT,K,F[104] 2Lab-TM/AdT,K,F[105,106] (Suitepagesuivan

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StudysiteSex/AgeclassDataReference(s) idemT,K[107] xLab-TM/AdT,K,F,EMG[108,109] 2Lab-TM/Juv&AdT,E[110,111] 5Lab-3T/3UM/Juv&AdT,K[112] 2TM&F/AdT,P[113] Macacafascicularis?Wild/habM/AdL,Po,H,ActX[114]3Lab-TM/J&AdEMG[28] 4/>7Wild/habM&F/AdL,H,travel[95] Macacamulatta242Wild/provM&F/InftoAdL,Po,H,ActX[16]1Lab-TF/AdT,K,F,EMG[40] PapiohamadryasidemT,F[42,44] 1Lab-T?/AdT,K[53] Papioanubis65Wild/hab32M&33F/InftoAdL,Po,H,ActX[115]10Encl-UM&F/InftoAdT,K[116,117] idemB,ActX[2]4Encl-TM&F/JuvT,K,F,EMG[118] ?Wild/hab?/AdL,Po,HX[34,35] 10Capt5M&5F/Inf-AdL,PoX[15] 22/65Capt11M&11F/InftoAdB,ActX[inprep] Theropitecusgelada?/?Wild/??/?B,ActX[20] Erythrocebus2Lab-U1M&1F/JuvEMG[119,120] Cercopitheucsdiana?Wild/habF/AdL,H,Act[121,122] Cercopithecus campbelli

?Wild/habF/AdL,H,Act[121] Cercopithecus ascanius

>20/?Wild/habM&F/AdL,Po,H,ActX[13] Cercopithecusmitis>20/?Wild/habM&F/AdL,Po,H,ActX[13] Cercopithecus aethiops

16Wild/??/InftoAdL,Po,H,rest[123] Cercocebusalbigena>20/?Wild/habM&F/AdL,Po,H,ActX[13] Colobinae Trachypithecus delacouri

27/72Wild/unhabM&F/Juv-AdL,Po,H,ActX[124] Colobusbadius?Wild/habF/AdL,H,Act[121,122] >20/?Wild/habM&F/AdL,Po,H,ActX[13] ?Wild/habM&F/AdL,Po,H,ActX[125] Colobusguereza>20/?Wild/habM&F/AdL,Po,H,ActX[13] ?Wildand Capt (2id)

?/?L,Po,H,ActX[126] (Suitepagesuivante)

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range of sizes and morphologies as well as varied locomotor specializations.

These study results show that the bipedal gait in non human catarrhines usually differs from that of humans in sev- eral respects, such as flexed hindlimbs, a trunk bent slightly forward, smaller bipedal strides and the single-humped profile of vertical ground reaction forces (for examples, see e.g. [29]

for a comparative description, and D ’ Août et al. in this vol- ume). Although very little data is available for Pongo, this species appears to be unique, with a gait initiated by a heel strike and an extended hindlimb, a relatively long stride and the double-humped profile of vertical ground reaction forces.

Besides these general differences compared to humans, experiments have demonstrated an unexpectedly wide diver- sity of bipedal gaits in these non human primates (in terms of spatio-temporal parameters as well as joint angles and mechanisms of foot contact to the ground), all performed in a well coordinated and non erratic manner, although these species are specialized for other locomotor modes and rarely use bipedal behaviour in their natural environment (e.g. see examples in D ’ Août et al., this volume).

Conclusion

This brief review highlights that bipedal behaviour among catarrhines, although occasional, is performed in a well coor- dinated and non erratic manner. There are many good rea- sons for comparing and integrating behavioural field-based data and laboratory-based experimental data. With regard to the evolutionary origin of habitual bipedalism, with the fossil corpus, this fundamental multidisciplinary knowledge sup- ports investigations into the possible functional precursors of habitual bipeds and the development of evolutionary sce- narios (for a recent contribution, see e.g. [1]).

In order to improve this fundamental knowledge by con- sidering a function in the ecological and behavioural con- texts of its use, the challenging task of translating labora- tory analyses into the field has been undertaken over several decades ([8]; see [131] on functional explorations).

With regard to the kinematics of primary locomotor modes, this can be done by means of video recordings (see e.g.

[132] on quadrupedal baboons). However, bipedal behav- iour has never been investigated experimentally in the wild;

its occasional nature and the constraints due to natural envi- ronmental conditions drastically limit the possibilities for experimental investigations of animals in the wild. From another point of view, lab-based experimental analyses do not take into account either the variety of bipedal behaviour patterns attested to in the wild, or the variety of contexts in which bipedalism can occur (types of support, activities, etc.). We believe that approaches integrating both lab-

StudysiteSex/AgeclassDataReference(s 19Wild/??/InftoAdL,Po,H,rest[123] 13+11Capt+Wild/ phab

?/?L,Po,HX[127] 12Wild/phab?/?L,Po,H,ActX[128,129] Colobuspolykomos?Wild/habF/AdL,H,Act[121,122] ?Wild/hab?/?Po,H,Act[130] Colobusverus?Wild/habF/AdL,H,Act[121] Studysite-incaptivity:Lab,laboratory;Encl,Enclosure;Capt,Captive(nodetails);T,Trained;U,Untrained;inthewild:hab,Habituated;unhab,Unhabituated;phab,PartiallyHabituated;prov,Provisioned Sex/Ageclass–M,Male;F,Female;Ad,Adult;Subad,Subadult;Juv,Juvenile;Inf,Infant Data–Biomechanicalstudy:T,Spatiotemporalparameters;K,Kinematics;F;Kinetics;P,Pedobarography;EMG,Electromyography;E,Energetics;Behaviouralstudy:L,Locomotion;Po,Posture;H,Habita Act,Activity;B,Bipedalismonly;Exp,Experimentalsetup Bipedalcomponent:X=walkingand/orstanding ?:noavailabledata.

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based and field experiments have great potential for addres- sing the full diversity of bipedal behaviour. For this pur- pose, animals living in a captive environment that is not too restrictive could provide good alternative models, inso- far as this (artificial) environment allows both the natural expression of their positional repertoire and easier access to the animals.

Acknowledgements: We are most grateful to the editor of the journal as well as to the anonymous reviewers for their comments on the first version of the manuscript.

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