RESEARCH ARTICLE

Degree of Terrestrial Activity of the Elusive Sun-Tailed Monkey(Cercopithecus solatus) in Gabon: Comparative Study of Behavior andPostcranial Morphometric Data

PEGGY MOTSCH1, GUILLAUME LE FLOHIC1,2, CAROLE DILGER1, ALEXIA DELAHAYE1,CARMELA CHATEAU-SMITH3, AND SEBASTIEN COUETTE4,5*1Unit�e de Recherche en �Ecologie et Sant�e, Centre International de Recherches M�edicales de Franceville (CIRMF),Franceville, Gabon2African Parks, Unit�e de Gestion, Service Conservation & Recherche, National Park of Odzala-Kokoua, Brazzaville,Republic of the Congo3UFR SVTE, Universit�e de Bourgogne, 6 Bd Gabriel, Dijon, France4UMR uB/CNRS 6282 Biog�eosciences, Universit�e de Bourgogne, 6 Bd Gabriel, Dijon, France5Laboratoire EPHE Pal�eobiodiversit�e et Evolution, Universit�e de Bourgogne, 6 Bd Gabriel, Dijon, France

We carried out a multidisciplinary study linking behavioral and morphological data from a little-known guenon species, Cercopithecus solatus, endemic to Gabon. Over a period of 9 months, wedocumented the pattern of stratum use associated with postural and locomotor behavior by directobservation (650hrs) of a semi-free-ranging breeding colony. We also conducted a morphometricanalysis of the humerus and limb proportions of 90 adult specimens from 16 guenon species,including C. solatus. Field observations indicated that C. solatus monkeys spent a third of their timeon the ground, similar to semi-terrestrial guenon species. We detected two patterns of stratum use: atground level, and in trees, at a height of 3–10m. The monkeys spent more time on the ground duringthe dry season than the wet season, feeding mainly at ground level, while resting, and socialbehaviors occurred more frequently in the tree strata. Our study of humerus size and shape, togetherwith the analysis of limb proportions, indicated morphofunctional adaptation of C. solatus to greaterterrestriality than previously thought. We therefore characterize C. solatus as a semi-terrestrialguenon, and propose a new hypothesis for the ancestral condition. By combining behavioral andmorphological results, we provide new information about the adaptive strategies of the species, andthe evolutionary history of guenons, thus contributing to the conservation of the sun-tailed monkey inthe wild. Am. J. Primatol. © 2015 Wiley Periodicals, Inc.

Key words: morphometrics; pattern of stratumuse; positional behavior; lifestyle; eco-morphology

INTRODUCTIONIn the animal kingdom, morphological traits are

strongly associated with ecological functions: infinches, beak morphological traits are inseparablefrom their diet [Grant & Grant, 1996] or vocalsignature [Badyaev et al., 2008; Podos, 2001]. Inmammals, cranial morphology and dietary ecologyare also associated [Christiansen & Wroe, 2007;Nogueira et al., 2009]. For example, in ungulates,horn morphology correlates with feeding and socialbehaviors [Janis, 1982]. Many biological aspects,from space use to biotic interactions (e.g.,competition, predation, and reproduction) are inti-mately related to morphological adaptations [Kay,1984]. Observation protocols, either in captivity or inthe wild, serve to determine to what extent morphol-ogy, and behavior interact [Wright, 2007]. It isnecessary to consider behavioral ecology andfunctional morphology together when assessing the

evolutionary history of species [Kaplin &Moermond,2000; Wright, 2007].

In the tribe Cercopithecini, which includesguenons, there is a great diversity of species, oftenliving in sympatry, and differing in their ecologicalniches. This diversity offers an excellent opportunityto study the relationships between ecology, morphol-ogy, and evolutionary history, given that small

Conflict of interest: None.

�Correspondence to: S�ebastien Couette, Laboratoire EPHEPal�eobiodiversit�e et Evolution, & UMR uB/CNRS 6282Biog�eosciences, Universit�e de Bourgogne, 6 Bd Gabriel, 21000Dijon, France.E-mail: sebastien.couette@ephe.sorbonne.fr

Received 3 September 2014; revision accepted 2 June 2015

DOI: 10.1002/ajp.22441Published online XX Month Year in Wiley Online Library(wileyonlinelibrary.com).

American Journal of Primatology

© 2015 Wiley Periodicals, Inc.

differences in ecology and behavior may coincidewithmorphological variation [Coward&McConathy,1996; Gebo & Sargis, 1994; Hurov, 1987; Kaplin &Moermond, 2000; McGraw, 2004; Rodman, 1979;Terrassin-Tholance, 1995; Wright, 2007]. Positionalbehaviors (i.e., postural and locomotor behaviors)and the degree of terrestriality (i.e., percentage oftime spent on the ground) in this tribe are intimatelyrelated to morphological traits [McGraw, 2004]. As aresult, studies of the evolutionary history of the tribeCercopithecini usually focus on locomotor andpostural abilities, and predict substrate preferencesby usingmultivariatemorphometrics, including limbproportions, and linear measurements of thepostcranial musculoskeletal system [Anapol, 2005;Escarguel, 2005; Manaster, 1979; McGraw, 2004;Ruff, 2002; Slice&Taylor 2005; Su&Jablonski 2009;Youlatos, 1999; Youlatos, 2003; Youlatos & Koufos,2010; Youlatos et al., 2012]. Ecological field studies,by contrast, often categorize species mainly bylifestyle (i.e., terrestrial, semi-terrestrial, or arbore-al), quantifying the degree of terrestriality todiscriminate between species [e.g., Gautier-Hion,1988]. Classifying activity budget and positionalbehaviors by the vertical stratum of the habitatwhere they occur provides a more comprehensiveanalysis of the pattern of stratum use (PSU),including the degree of terrestriality. Such ecologicalfield study more clearly identifies substratepreferences and their ecological determinants (e.g.,food resources).

In-depth knowledge of the lhoesti superspecies,which includes three species, Cercopithecus lhoesti,C. preussi, and C. solatus, is important forunderstanding the evolutionary history of the tribeCercopithecini. The lhoesti group is associated with aterrestrial lifestyle, whereas most other guenonspecies (other than Cercopithecus aethiops andErythrocebus patas) are generally considered to bearboreal and forest-dwelling [Fleagle, 1999; Gautier-Hion, 1988; Gebo & Sargis, 1994]. The adaptation ofthe Cercopithecus lhoesti group to a terrestriallifestyle appears to be concomitant with morphologi-cal adaptations [Fleagle, 1999]. Cercopithecuslhoesti, C. preussi, and C. solatus are remarkableamong guenon species for their distinctive behavior-al and ecological characteristics, as well as theirdisjointed and restricted distribution, and theirsmall populations [Kaplin & Moermond, 2000].Such small populations mean that data pertainingtomorphological analyses and behavioral studies arerare for the lhoesti group, especially for C. solatus[Kaplin & Moermond, 2000]. In many major studiesand reviews [Ankel-Simons, 2000; Cardini & Elton,2008; Delson et al., 2000; Fleagle, 1999; Gebo &Sargis, 1994; Senut, 1986; Smith & Cheverud, 2002],C. solatus is either entirely absent from datasets orconsiderably underrepresented, compared to otherguenon species.

The sun-tailed monkey, C. solatus, is endemic toGabon, where it was first discovered in 1984[Harrison, 1988]. The cryptic nature of the specieshas limited direct observation in the wild. Mostecological data come from brief informal observationsmade when the species was first discovered [Gautier-Hion, 1988; Harrison, 1988]:C. solatus is described asa species that forages on the ground for plantmaterial, fruits, and invertebrates, spending about40% of its time there. However, these initial studies,though of primary importance, relied mostly onopportunistic or indirect observation. Laterobservation of semi-free-ranging monkeys suggestedthat the degree of terrestriality ofC. solatuswasmorethan twice as high as the values published byGauthier-Hion [1988], and the lifestyle category wasrevised from semi-terrestrial to terrestrial [Peignotet al., 2000]. Such conflicting assessments of thedegree of terrestriality highlight the need for a morecomprehensive characterization of PSU forC. solatus.

The collection of new data on the ecology of C.solatus has been in progress since 2009, as anongoing component of the ECOSOL project (Ecologyand Conservation of Cercopithecus solatus). Part ofthis vast collection of behavioral ecological field dataenabled us to calculate the degree of terrestriality ofC. solatus, and also to investigate PSUand positionalbehavior. Taking into account ecological determi-nants (i.e., seasonality) of PSU, we compiled a fullecological profile for C. solatus. We compared theseresults with the profiles of 19 other Cercopithecinispecies, based on data obtained from the literature.Aftermorphometric analysis of long bones fromadultsun-tailed monkeys and 15 other guenon species, weused two distinctmultivariate analyses to predict thesubstrate preference of C. solatus.

MATERIALS AND METHODSDefinition of Terms Used

In Table I, we define the terms used in this paperto avoid confusion. Consistent use of some termsremains problematic in the literature.

Behavioral StudyOur research complies with protocols approved

by the Animal Research Ethics Committee of thePrimatology Center at the Centre International deRecherches M�edicales de Franceville (CIRMF), andadheres to Gabonese legal requirements, and to thePrinciples for the Ethical Treatment of Non-HumanPrimates defined by the American Society ofPrimatologists.

Study group and rainforest enclosureThe study group of semi-free-ranging sun-tailed

monkeys was a breeding group with 13 individually

Am. J. Primatol.

2 / Motsch et al.

recognized members: one adult male, six adultfemales, and immatures of both sexes. Thishabituated group lived in a 0.7-ha rainforest enclo-sure, where they foraged freely on natural leaves,fruits, roots, bark, seeds, stems, and insects [Peignotet al., 2000 and personal observation]. The naturaldiet was supplemented with bananas, wild fruits,and soya-based homemade cake twice a day. Waterwas available ad libitum.

The enclosure consisted of a degraded secondaryforest, with very dense undergrowth comprisinglianas and shrubs. Several plant species characteris-tic of the surrounding primary lowland rainforestwere present, including trees (Burseraceae:Aukoumea klaineana and Santiria trimera, Legumi-nosae-Mimosoideae: Penthacletra macrophylla,Euphorbiaceae: Uapaca guineensis, Annonaceae:

Xylopia aethiopica) and lianas (Gnetaceae: Gnetumafricanum, Euphorbiaceae: Manniophyton fulvum,Connaraceae: Cnestis sp.). Other plants characteris-tic of degraded forests were also present (e.g.,Arecaceae: Elaeis guineensis, Moraceae: Musangacecropioides). The canopy averaged 15–20m high,with a maximum height of approximately 25m.Leaves generally covered the ground. A securityperimeter, approximately 3m wide, free of trees andcovered by herbaceous species, ran along the inside ofthe boundary fence.

Behavioral data collectionTwo researchers (AD and CD) collected

behavioral data from dawn to dusk, 6 days permonth, from April to August 2011, and fromSeptember to December 2012 (total observations:

TABLE I. Definition of the Terms Used in this Publication.

Terms used Definition

Degree of terrestriality The degree of terrestriality refers to the percentage of time an animalspends at ground level.

Lifestyle ”Lifestyle” refers to the general categorization of ecology and behaviour ofa species. Herein, we consider three different lifestyles displayed byprimates, depending on the proportion of time spent in each habitatstratum: an “arboreal” lifestyle category fits for species using mostlynon-terrestrial canopy, whereas a “terrestrial” lifestyle category fits forspecies using the ground for most (>50%) of their activities. A“semi-terrestrial” lifestyle fits species that spend 20-40% of their timeon the ground Gautier-Hion [1988].

Pattern of strata use (PSU) PSU is a profile of the time spent in every chosen stratum, and is be amore comprehensive representation of ecology than lifestyle alone.Thus, the pattern of strata use integrates components of behaviour,such as social relationships or diet. It facilitates the identification ofmultimodal use of the vertical habitat without predeterminedassumptions.

Substrate preference Substrate preference refers implicitly to the use of substrate resourcesproportionally higher than their availability, and needs to be shownstatistically to determine a non-random use of habitat. However,availability of strata is a very difficult parameter to assess, particularlybetween sites or segments of a study area. Therefore, the termsubstrate preference is used here as a prediction made after analysis ofthe morphological traits of animals. The prediction refers to aconsideration of which substrates are more likely most efficientlyutilized with a given morphology.

Locomotor behaviours or abilities In behavioural ecology studies, locomotor behaviour corresponds to anindividual’s pattern of movement, such as bipedal, quadrupedal orcling-and-leaping locomotion, as well as the classification of specificsets of movements including running, walking or leaping. From amorphological perspective, locomotor abilities may also be predictedbased on the association between specific morphology and comparativebehavioural data.

Postural behaviours or abilities In behavioural ecology studies, postural behaviours correspond to thepositions an individual assumes during bouts of immobility (forexample, during resting, feeding or foraging bouts). In morphologicalstudies, postural abilities refer to the predicted capacity to exhibit suchpostural behaviours inferred from comparative skeletal data.

Positional behaviours or abilities Prost [1965] ortotal locomotor pattern Ripley [1967]

All these terms refer to the overall combination of locomotor and posturalbehaviours (or abilities) that an animal exhibits, and are both relatedto a general interpretation of adaptation or lifeway Martin [1990].

Am. J. Primatol.

Semi-Terrestriality of Cercopithecus Solatus / 3

>650hr, 16,862 scans; monthly individual observa-tion: mean¼39.2� 16.4 hrs, 95%CI¼ [35.8–42.5],N¼93). Observations took place within theenclosure, generally at a distance of 3–10m fromthe animals. Using the “instantaneous scan” sam-pling method [Altmann, 1974] at 10-min intervals,the observer scanned from left to right, for amaximum of two minutes, to record the behavior ofthe first five individuals seen.

The five classes of activity were feeding, foraging,traveling, social interactions (agonistic and affilia-tive), and resting. Feeding describes the act of eating,whereas foraging describes the search for food (e.g.,scratching theground, turningover stones).Travelingdescribes all locomotor behaviors: bipedal and qua-drupedal running and walking, leaping and climbing(following definitions in McGraw, 1996). We alsoincluded “solitary locomotor play” (solitary energeticplay behaviors, e.g., playing while hanging from abranch) as traveling. Resting comprised all posturalbehaviors: sitting, quadrupedal posture, lying, andsprawling (i.e., lying prone, following the definition inMcGraw, 2000); it also comprised quiet solitary playbehaviors (e.g., playing gently while seated).

Data analysisWe defined four forest strata to analyze the

pattern of stratum use (PSU): 1) “ground level” at0m, 2) “lower stratum” <3m, 3) “medium stratum”3–10m, and 4) “higher stratum” >10m. We thencompiled locomotor and postural behavioral profilesfor C. solatus. To avoid potential bias, we excludedfrom our analysis any records in which animals werefeeding on provisioned food.

We also calculated seasonal differences inactivity budget within each stratum, to bettercharacterize PSU for C. solatus. We classified theseasons according to normative patterns for Gabon[Hijmans et al., 2005]. The wet season groupedtogether themonths of April andMay and Septemberto December, while the dry season included themonths from June to August.

Statistical analysesWe carried out statistical analyses using SPSS

(version 17.0 for Windows; SPSS, Chicago, IL). Asthere were slight differences in sample size amongindividuals and in observation time across seasons,we weighted the data by the number of scans perindividual, per hour of the day and per month (thuscorrecting for unequal observation effort), prior tothe analysis. This process led us to create 93comparable statistical individuals (i.e., individual�month records), which represented repeatedmeasures of 15 individuals for 9 months (135observations), minus the 42 observations for whichspecific individuals were not recorded (newborns,dead or injured during the study). In our analyses,each of the 93 data points was a single individual per

month, with the same individual being consideredeach month. We used paired Student t tests tocompare wet and dry seasons for PSU. Repeatedmeasures analysis of variance (ANOVA) comparedthe five behavioral activities (feeding, foraging,traveling, social interactions and resting) accordingto season and stratum use. Pairwise comparisonsused post hoc tests with �Sid�ak correction. Weconsidered results significantly different at P<0.05.

Morphometric StudyMorphometric measurements and analyses

Morphometricmeasurements came from90adultguenon skeletons (Table II). Specimens originatedfrom collections at the Mus�eum national d’Histoirenaturelle (MNHN, Paris, France), the Natural Histo-ry Museum (NHM, London, UK), and the AmericanMuseum of Natural History (AMNH, New York).Postcranial and cranial materials were associated inthe collections, and we assessed the maturity ofspecimensbased on the fusion of epiphyseal cartilagesand eruption of third molars. We sampled only sexedspecimens with intact stylopods and zeugopods (nomissing bones or breakage).

Wemeasured 13morphometric variables on limbelements (Fig. 1, Table III), using a digital caliperwith a precision of 1mm.We corrected for the effect oflimb size using the Burnaby procedure, whichconsists of extracting an isometric vector from themultivariate dataset and computing new datacoordinates in a subspace that is orthogonal to thisvector [Burnaby, 1966].

Morphometric multivariate analysesWe tested for size differences within our sample,

particularly sexual dimorphism, which we corrected

TABLEII. Numberof SpecimensperTaxonbySex.WeFollowed the Classification of Grubb et al. [2003].

Genus Species Males Females

Cercopithecus nictitans 5 5mona 3 2cephus 4 4neglectus 1 —

lhoesti 6 4solatus 1 3diana 2 3hamlyni 1 —

pogonias 5 4erythrotis 1 —

ascanius 2 2mitis 2 5

Chlorocebus aethiops 1 6Miopithecus talapoin 2 4Allenopithecus nigroviridis 3 1Erythrocebus patas 3 5

Total 90

Am. J. Primatol.

4 / Motsch et al.

when differenceswere significant betweenmales andfemales within species. We predicted positionalabilities and substrate preference of C. solatus basedon arm morphology, using multivariate analysis ofhumeral measurements. We used the literature toidentify the lifestyle of each of the other 16 speciesincluded in the analysis (Table IV). We performed a

Discriminant Function Analysis, followed by aCanonical Variate Analysis, on 86 specimens (allsamples, minus the 4C. solatus specimens), withsubstrate preference to define the groups. Thisestablished a predictive model that allowed us toassign the C. solatus specimens to the most likelysubstrate preference group. We used R version 2.12

Figure 1. Morphometric variables used in this study. On the left, humeral linear measurement used for themultivariate morphometricstudy. On the right, forelimb, and hind limb segment dimensions used for the regressions. For measurement definitions, see Table III.

TABLE III. Morphometric Measurements Involved in this Study. The Measurements are Based on the Ones Usedby Youlatos et al. [2012]. Refer to Figure 1 for Illustrations of these Measurements.

Variable Name Definition

HHH Humeral head height Maximum diameter of the headHHW Humeral head width Transverse diameter of the headOLL Olecranon fossa

lengthMaximum diameter of the olecranon fossa

OLW Olecranon fossa width Transverse diameter of the olecranon fossaTRL Trochlea length Maximum length of the trochlea taken in antero posterior planeARTW Distal articular width Maximum medio-lateral diameter of the trochlea and capitulum taken perpendicular to

shaft.BIEPW Biepicondylar width Maximum medio-lateral diameter perpendicular to shaft between tips of epicondylesHL Humerus length Distance from head to capitulumUL Ulna length Proximalmost end of the olecranon to headRL Radius length Distance from the head to the most distal part of the styloid processFL Femoral length Distance from head to medial condyleTL Tibia length Distance from the head to the distal part of the internal malleolusFBL Fibula length Distance from head to lateral malleolus

Am. J. Primatol.

Semi-Terrestriality of Cercopithecus Solatus / 5

(MASS [Venables and Ripley, 2002] and Candisc[Friendly and Fox, 2013] packages) for theseanalyses.

We assessed the positional behavior of sun-tailedmonkeys by computing indices from limb propor-tions. These indices are commonly used to assess thelocomotor pattern of primate [e.g., Napier & Napier,1967; Schultz, 1969]. We calculated a median valueper species for each variable. We chose to work withmedian values rather than means, both to takeaccount of the small sample size, and because themedian is less affected by extreme values. Wecomputed pairwise correlations between limb seg-ment lengths, using R (base package). We performedmajor axis regressions, and calculated associatedstatistics (slope, 95% confidence index of slope,intercept and coefficient of determination).We testedfor scaling (isometry vs. allometry) following theprocedure of Claude [2008]. Our statistical analysiswas based on that published by Sargis et al. [2008]; tofacilitate direct comparisons of results.

RESULTSBehavioral StudyTime spent on the ground and the pattern ofstratum use

The PSU for C. solatus was as follows: only1.5�0.9% of time was spent in the higher

stratum; 39.3�10.1% in the medium stratum;25.5�2.8% in the lower stratum; while the timespent on the ground was 33.7�10.4% (N¼ 93statistical individuals). Comparisons between C.solatus and other guenon species were basedsolely on the relatively sparse data available forthe time spent on the ground (Table IV). The timespent on the ground for C. solatus (33.7%, 4.04hours a day) more closely resembles that of semi-terrestrial species (15.2–38%) which is far lowerthan in terrestrial species (almost 60% for E.patas, Table IV).

Seasonal variationC. solatus used the medium and higher strata in

the wet season significantly more often than in thedry season (Fig. 2, respectively t¼ 2.906, P¼0.023and t¼3.321,P¼0.013), while ground level was usedin the wet season significantly less often than in thedry season (t¼3.202, P¼0.015). There was nosignificant seasonal difference in use of the lowerstratum.

We examined seasonal variation for PSU inrelation to behavioral activity (Table V) and foundsignificant effects of season (F(5,85)¼3.584,P¼ 0.009), of PSU (F(12,251)¼ 12.506, P<0.001),activity (F¼8.5, P<0.001) and their interaction(F(12,251)¼2.128, P¼0.016). Post hoc tests indicatedthat most feeding occurred at ground level in bothseason, it increased significantly from 50.2% in the

TABLE IV. Life Style and Time Spent on the Ground of Different Guenon Species. (The Source Given for EachSpecies is What we Considered as the Main Publication or the Major Synthesis on this Topic).

Taxon TSG (%) Environment Life style References

C. petaurista <1 WLD Arboreal McGraw [2000]C. diana� 1.7 WLD Arboreal McGraw [2000]A. nigroviridis

�,a 90 WLD Semi-terrestrial? Gautier [1985]; Gautier-Hion [1988]C. hamlyni

� ,b — — Semi-terrestrial? Gebo & Sargis [1994]; Cardini & Elton [2008]C. erythrotis� — WLD Arboreal Gonzalez-Kircher [1996]C. ascanius� — WLD Arboreal Gebo & Chapman [1995]C. mona

�,c — — Arboreal Gebo & Sargis [1994]C. mitis� 9 WLD Arboreal Gebo & Sargis [1994]; Gautier-Hion [1988]C. pogonias� <2 WLD Arboreal Gautier-Hion & Gautier [1974]C. nictitans� <3�� WLD Arboreal Gautier-Hion [1988]M. talapoin� 5 WLD Arboreal Gautier-Hion [1988]C. cephus� 11 WLD Arboreal Gautier-Hion & Gautier [1974]C. campbelli 15.2 WLD Semi-terrestrial McGraw [2000]C. aethiops� 20 WLD Semi-terrestrial Rose [1979]C. neglectus� 30 WLD Semi-terrestrial Quris [1976]; Gautier-Hion [1988]C. preussi 35 WLD Terrestrial Gautier-Hion [1988]C. lhoesti� 38 WLD Semi-terrestrial Struhsaker [1981]C. solatus� 33.7 SFR ? Present studyC. solatus 40 WLD Semi-terrestrial Gautier-Hion [1988]E. patas� 59.6 WLD Terrestrial Isbell et al. [1998]C. solatus 85.5 SFR Terrestrial Peignot et al. [2000]

SFR, Semi-Free-Ranging; WLD, Wild; TSG, Time spent on the ground. �Guenon species considered in this study; ��time spent under 10m high.(a) based on sparse data, in Gautier-Hion [1988]; based on 2 specimens, in Gebo and Sargis [1994](b) defined as semi-terrestrial, in Gebo and Sargis [1994] but as arboreal, in Cardini and Elton [2008](c) based on a single specimen, in Gebo and Sargis [1994]

Am. J. Primatol.

6 / Motsch et al.

wet season to 83.7% in the dry (P<0.001). Converse-ly, feeding time in the lower and medium stratadecreased significantly from 21.7% to 8.1%(P<0.001) and from 27.1% to 7.8% (P<0.001),respectively. Traveling and resting showed similarpatterns: traveling time at ground level increasedsignificantly from35.6% in thewet season to 50.4% inthe dry season (P< 0.001), while resting timeincreased significantly from 13.1% in the wet seasonto 27.3% (P<0.001) in the dry season. Conversely,traveling and resting time in the medium stratadecreased significantly from 39.0% to 24.9%(P<0.001) and from 50.0% to 35.6% (P<0.001),respectively. Traveling and resting showed similarpatterns: traveling time at ground level increasedsignificantly from35.6% in thewet season to 50.4% inthe dry season (P< 0.001), while resting timeincreased significantly from 13.1% in the wet seasonto 27.3% (P<0.001) in the dry season. Conversely,traveling and resting time in the medium stratum

decreased from wet to dry seasons from 39.0% to24.9% (P< 0.001) and from 50.0% to 35.6%(P<0.001), respectively. Foraging time in the medi-um stratum decreased from 31.1% to 22.1%(P< 0.001) but there were no significant seasonaldifferences in other strata. For the higher stratum,values were always low, but significantly higher fortravel, rest and social behavior in the wet season. Wefound no significant difference for the lower stratum,whatever the activity.

Locomotor and postural behaviorWe compiled the profile of locomotor behaviors

using only behaviors included in “travel activity”:quadrupedal locomotion (walking and running)represented 57.2% of the time, leaping 17.2%,climbing 23.5%, and bipedal locomotion 2.2%(N¼93 statistical individuals).

The profile of postural behaviors included onlybehaviors classified as “resting”. Sitting accounted

Figure 2. Seasonal patterns in the use of different strata for C. solatus. Significant differences between seasons are identified byasterisks. Bars represent means and standard errors.

TABLE V. Distribution of Every Activity Among the Strata and Comparison Between Dry and Wet Season.

Ground level Lower stratum Medium stratum Higher stratum

Wet SeasonFeeding 50.2� 21.7� 27.1� 1.2Foraging 51.9 15.6 31.1� 1.4Travel 35.6� 22.9 39.0� 2.6Social 15.7� 20.5 61.6� 2.1Rest 13.1� 35.1 50.0� 1.7Dry SeasonFeeding 83.7� 8.1 7.8 0.3Foraging 55.3 21.8 22.1� 0.7Travel 50.4� 24.2 24.9� 0.5Social 31.0� 24.3 45.0� 0.1Rest 27.3� 36.3 35.6� 0.7

At a given season, the number is the proportion of activity records in a given activity category that occur in each stratum. �represents significant differencesin the given activity between dry and wet season (P< 0.05) with the post;

Am. J. Primatol.

Semi-Terrestriality of Cercopithecus Solatus / 7

for 84.1% of resting time (with self-groomingrepresenting 8.0% of this), quadrupedal standing10.6%, lying 2.8%, and sprawling 0.1%.

Morphometric StudyWe tested for the effects of species and sex on

humeral measurements, using a two-way ANOVA.We found a significant effect for species (F¼ 1.7,P<0.05), but not for sex (F¼1.2, P¼0.317), nor forthe interaction between the two factors (W¼ 0.792,P¼0.496). Discriminant Function Analysis (DFA)identified two functions accounting for 81.1% and12.2% of the total variance (Table VI). Using thesetwo functions, only 9.7% of the specimens weremisclassified. The scatterplot of the CanonicalVariate Analysis after DFA (Fig. 3) presents thegrouping of substrate preference along function 1(CV1). Positive CV1 values characterize humeri witharticular epiphyses that are broader (medio-lateraldimension) than they are high (proximo-distaldimension). Negative values characterize epiphysesthat are high (proximo-distally) and narrow(medio-laterally). The CV1 axis (which accounts for81.1% of the variation) discriminates arborealspecies (negative values) from terrestrial ones(positive values). Semi-terrestrial species have anintermediate position along this axis. The CV2 axis(accounting for 12.2% of the variation) does not seem

to discriminate substrate preference groups, and it isdifficult to identify grouping trends along this axis.

Following computation of post-hoc comparisons,we classified two C. solatus specimens as terrestrial(57% and 63%), while the other two were classified assemi-terrestrial (83% and 87%). These results indi-cate that C. solatus humeri display charactersattributed to both terrestrial and semi-terrestrialactivities.

Limb proportion relationships (Table VII) werewell described by a linear model with relatively highdetermination coefficient values (up to 90%). All

TABLE VI. Loadings of the Eight MorphometricVariables on both Discriminant Functions. The Anal-ysis is Performed on 86 Specimens and the Specimensare Grouped by Substrate Preferences.

Variables Function 1 Function 2

HHH 1.5214 �0.3716HHW �0.4367 �0.3185OLL 1.3185 �0.4291OLW �1.9882 0.2341TRL 2.3102 �0.5274ARTW �2.4429 �0.2383BIEPW �1.9962 0.5123HL �0.3967 �0.2008Eigenvalues 0.5612 0.1157% of variation 0.81126 0.12461

Figure 3. Biplot of Canonical Variate scores obtained after discriminant analysis of the eight size-adjusted humeral morphometricvariables. Discriminant Function analysis used substrate preference for group variable. DFA was run on the entire sample withoutC. solatus and the sun-tailedmonkey specimenswere assessed separately. Table VI presents variable loadings and functions eigenvalues.

Am. J. Primatol.

8 / Motsch et al.

correlationswere isometric, affecting both hind limbsand forelimbs to the same extent. Figure 4 presentsbrachial (Fig. 4A) and intermembral (Fig. 4B) indi-ces. The distinction between arboreal (low values),semi-terrestrial (intermediate values) and terrestri-al (high values) was clearly visible in both bivariateplots. This group distinctionwas particularly evidentin the intermembral index (Fig. 4B). The position ofC. solatus along the linear model suggested a highproportion of terrestrial activities - higher than in allthe species classified as semi-terrestrial. The degreeof terrestriality of C. solatus was, however, lowerthan that of the most terrestrial species, E. patas.

DISCUSSIONSince captivity may alter natural behaviors

[Birkett & Newton-Fisher, 2011; Hosey, 2005;Khan, 2013; Nowak et al., 2014], it is essential toevaluate to what degree the environment of the focalgroup can be considered natural. Our study grouplives under natural climatic conditions, identical tothose in the wild. Although both the diversity andrelative abundance of the plant species in theenclosure do not match what occurs in the wild,many species are present within the geographicrange of C. solatus,which consists mainly of primarylowland rainforest [Brugi�ere et al., 1998; Harrison,1988] with some secondary forest areas [Gautieret al., 1992]. In the wild, degraded vegetation doesnot seem to affect the abundance of C. solatus, whichis even able to live close to villages and plantations,where the dense undergrowth enables the monkeysto move cryptically [Gautier et al., 1992; Motschet al., 2011; PM, personal observation]. In thishabitat, similar to our enclosure, C. solatus feedson species such asMusanga cecropioides, at the edgeof the forest alongside the road [Motsch et al., 2011],or on crops (PM, unpublished data). Furthermore,with the exception of leopards (Panthera pardus),most of the presumed natural predators of C. solatusand other Central African guenons have been seen inthe enclosure, including snakes, such as the python(Python sebae) and Gaboon viper (Bitis gabonica),

and birds of prey, including the crowned eagle(Stephanoaetus coronatus). Although the home rangesize of a wild group of C. solatus is not known, itwould probably not exceed 1–2km2 based on thehome range size of other guenon species [Clutton-Brock & Harvey, 1977], including C. lhoesti [Kaplin,2001]. Therefore, horizontal space use in the enclo-sure may well be different from what occurs in thewild. Nevertheless, this group appears to be the besttool available to study the behavioral ecology of aspecies whose cryptic nature renders habituation inthe wild very unlikely, so that study or even directopportunistic observations remain extremely rare(JP Gautier, personal communication).

Behavioral studyLifestyle

The two previous analyses focusing on thelifestyle of C. solatus came to different conclusions[Gautier-Hion, 1988; Peignot et al., 2000]. Both,however, showed C. solatus to be among the mostterrestrial of Cercopithecus species. The locomotorcharacterization of a species is often ambiguousbecause it is based on observations performed invarious conditions. The frequently cited work ofGautier-Hion [1988] is the major reference for theCercopithecus solatus locomotor pattern, yet nolifestyle categorization was provided in that study.In several studies citing Gautier-Hion’s work, C.solatus is grouped with C. preussi and C. lhoesti assemi-terrestrial or terrestrial species, yet surpris-ingly, Soligo and Martin [2006] classified C. solatusas an arboreal guenon species. We agree that it is fartoo simplistic to attempt to categorize a species underone narrowly defined lifestyle [see also Senut, 1991].Even though intermediate categories exist betweenarboreality and terrestriality, these two terms arestill not clearly defined. Nevertheless, our results areconsistent with the time spent on the ground of 40%given in Gautier-Hion [1988]. We therefore considerthe focal group in our study as semi-terrestrial, witha value for time spent on the ground of 33.7%, and59.2% for the time spent below3meters. Althoughwe

TABLE VII. Reduced Major Axis Statistics for Regressions of Size Corrected Limb Segment Lengths onto others.

Slope 95%CI slope y intercept R2 N Scaling

Humerus versus Radius 1.29 1.25–1.36 �0.0024 0.92 16 IsometricHumerus versus Ulna 1.33 1.099–1.47 0.083 0.89 16 IsometricHumerus versus Femur �1.18 �0.993 to �1.227 0.107 0.93 16 IsometricFemur versus Tibia 0.98 0.883–1.112 0.004 0.95 16 IsometricFemur versus Fibula �1.01 �0.912 to �1.088 �0.071 0.94 16 IsometricRadius versus Tibia �0.877 �0.731 to �1.101 0.021 0.92 16 IsometricRadius versus Fibula �0.782 �0.703 to �0.881 �0.041 0.88 16 IsometricUlna versus Tibia �0.121 �0.981 to �1.284 0.079 0.96 16 IsometricUlna versus Fibula �0.704 �0.681 to �0.801 0.036 0.95 16 IsometricHind limb versus Forelimb �1.014 �0.873 to �1.151 �0.021 0.99 16 Isometric

Am. J. Primatol.

Semi-Terrestriality of Cercopithecus Solatus / 9

observed sun-tailed monkeys in the same site asPeignot et al. [2000] with similar living-conditionsand social structure, our estimation of time spent onthe ground is far lower than the 85.5% value theypublished. We suspect that this difference arosebecause Peignot et al.’s observations focused on openareas, where C. solatus individuals were easilyvisible from the outside of the enclosure. In ourstudy, observers followed the monkeys into theforest. The time spent on the ground for C. solatuswas similar to that of the two other species of the C.lhoesti group (C. lhoesti, 38% and C. preussi, 35%).The comparisonwith the time spent on the ground forother guenons highlights the semi-terrestrial char-acter of the C. solatus lifestyle.

Pattern of stratum use and ecologicaldeterminants

The quantification of time spent on the ground isa good proxy for characterizing species lifestyles.However, it does not take into account posturalbehaviors or the pattern of stratumuse and thusmaynot be precise enough to characterize speciesbehavior.

Our results show that Cercopithecus solatusmainly used two strata: ground level, and themedium stratum (between 3 and 10m). We pre-sumed, therefore, that these two strata wouldprovide the majority of resources for this species.Analysis of the activity budget suggested that groundlevel provides food resources, while the mediumstratum provides shelter and space to rest andinteract with conspecifics. Although the group usedground level more often in the dry season, activitieswere not greatly modified on a seasonal basis (i.e.,:the activity budget for each stratum remainedstatistically unchanged), suggesting that energyexpenditure and resource use are fairly constant.

As behavior in the lower stratum and higher stratumremained unchanged across the seasons, we hypoth-esize that C. solatus displays two types of PSU, withprobable variation in resource quality (nutrientcontent, abundance and/ or availability of food items)between seasons explaining the variation in timespent on the ground. In fact, PSU shifts seasonally,with time spent on the ground increasing during thedry season.

Feeding appears to be the only activity for whichsignificant inter-seasonal difference in time spent onthe ground occurred (i.e.,: considering the PSU foreach activity). Feeding time at the ground levelincreased by 16.1% during the dry season: thisincrease appeared to be associated with food gather-ing, as well as feeding, at this level. Since there isregular provisioning of fruits, the group may climbdown to the ground level more frequently during thedry season, when fruits are less available in thehigher strata [White, 1994]. Other resources (fallenfruits, herbaceous leaves and stems, invertebrates)may also be foraged on the ground. Further ecologicalinvestigations on seasonal variation in diet composi-tion in a non-supplemented environment could shedlight on human-influenced behaviors in comparisonwith natural behaviors [Nowak et al., 2014].

Locomotor behaviors for C. solatus demonstrateterrestriality more frequently than arboreality,using the categories defined by Fleagle [1999] withhigh frequencies for quadrupedal running andwalking and low frequency for leaping. In addition,postural behaviors of the group were generallysimilar to the more terrestrial species of guenons,with a high proportion of quadrupedal standing andlow proportions of lying and sprawling (which areexpected to be more frequent in tree strata).However, statistical analyses were not possible dueto the lack of comparative data. This first overall

Figure 4. ReducedMajor Axis regressions of some size-corrected membral segment dimensions. A: illustration of the brachial index (logsize-corrected radius length/ log size-corrected humerus length); B, illustration of the intermembral index (log size-corrected forelimblength /log size-corrected hind limb length). See Table VII for complementary statistics.

Am. J. Primatol.

10 / Motsch et al.

representation of stratum use by C. solatus coupledwith comparisons to other guenon species underlinesthe semi-terrestrial rather than arboreal character ofthe speciesC. solatus, as is also the case forC. lhoesti[Kaplin &Moermond, 2000] and C. preussi [Gautier-Hion, 1988].

Morphometric AnalysesAlthough captivity can affect species behavior,

Bello-Hellegouarch et al. [2013] demonstrated that ithas no effect onmorphology. In any case, a semi-free-ranging colony lives in very different conditions thananimals in captivity.

Sexual dimorphism appears to have no signifi-cant effect on humerus morphology. As concluded bySenut [1986] using a sample of extant haplorhines,the distinction of sexes based on long bone morphol-ogy remains very difficult if not impossible. Ourresults corroborate Senut’s conclusions and indicatethe absence or low degree of dimorphism in guenonhumerus morphology. However, the number ofspecimens in Senut’s sample for Cercopithecinispecies was quite small (eleven specimens for thegenus Cercopithecus).

Multivariate analyses on morphometric varia-bles indicate clear differences in humerusmorphology between species considered as arboreal,semi-terrestrial and terrestrial (using classificationsgathered from comparable literature). The humeralheads of arboreal species are rounded, while thedistal epiphyses are broader (medio-laterally) thanthey are high (proximo-distally). In contrast, terres-trial species have long humeri with narrow heads,proximo-distally developed tuberosities (limitinglateral movement of the arm) and distal epiphysesthat are higher (proximo-distally) than they are wide(antero-posteriorally). In terms of functional mor-phology, a rounded humeral head allows movementof the shoulder in multiple directions, whereas ahigh, narrow head suggests restriction of shouldermovement to an antero-posterior axis [Larson &Stern, 1989]. Movement is also restricted by theposition of the coracoid process of the scapula and bythe tuberosities of the humeral head. Wide distalepiphyses (described by the variables Distal Articu-lar Width, Olecranon Width, Biepicondylar Width,and Trochlea Width) attest to lateral movements ofthe elbow as well as mobility during pronation andsupination [Jenkins, 1973]. In contrast, high distalepiphyses (the variables Trochlea Length, andOlecranon Length) characterize humeri with re-stricted elbow movement and enhanced stability ofthe forearm during quadrupedal walking. Thetrochlea is developed, limiting the lateralmovementsof the ulna and supporting antero-posterior move-ments [Oxnard, 1963]. These lateral movements arealso limited by the association of a large olecranonprocess and a deep olecranon fossa (variable OLL).

These morpho-functional interpretations are consis-tent with previous studies linking humerus mor-phology to substrate preference in primates [Fleagle& Simons, 1982; Gebo & Sargis, 1994; Jolly, 1965,1967, 1972; Rose, 1988; Su & Jablonski, 2009]. Thecombination of our behavioral and morphometricanalyses indicates a high proportion of terrestrialactivities for Cercopithecus solatus—higher than forCercopithecus lhoesti but lower than for the veryterrestrial Erythrocebus patas. Likewise, our mor-phometric results corroborate ecological findings andindicate that (1) C. preussi and C. lhoesti could beconsidered as semi-terrestrial species, and (2) withinthe C. lhoesti group, C. solatus is the most terrestrialspecies.

In 2000, Groves saw themorphological similaritybetween Cercopithecus aethiops and Erythrocebuspatas and proposed to group the species in the samegenus Chlorocebus. In 2006, Groves suggestedgrouping the lhoesti group in the new genusAllochrocebus and then distinguishing the threespecies in the group from the other terrestrial speciesof the clade. These taxonomic propositions werebased on phylogenetic results. Although terrestriallocomotion is very important in the clade, we canneither confirm nor reject these propositions. Theanalysis of morphological variation was not con-ducted within a phylogenetic framework but ratherto be compared to phylogenetic hypotheses.

A recurrent problem in behavioral studies is thefact that the categories ‘terrestrial’ and ‘arboreal’ arenot mutually exclusive. The term ’semi-terrestrial’describes an intermediate condition, but even threelevels are not sufficient to characterize substratepreference associated with positional behaviors andmorphological abilities. The definitions of theseclasses are vague and the attribution to a givencategory is inevitably subjective. Terrassin-Tholance[1995] further refined these categories by addingvegetation type to the behavior (e.g., savanna semi-terrestiality). However, there is still potential forfurther study of type of locomotion, patterns ofstratumuse, and associated behaviors. Asmentionedpreviously, the degrees of terrestriality for C. solatusreported in Gautier-Hion [1988] and in Peignot et al.[2000] are highly divergent, leading to very differentcharacterizations of substrate preference. This isalso the case for other guenon species, such asCercopithecus aethiops (see Table 16.2 comments inSargis et al. [2008]), C. hamlyni and A. nigroviridis(see Table IV comments). Under these circumstan-ces, it is necessary to test several approaches (e.g.field observations and morpho-functional analyses),to improve substrate preference hypotheses.

The link between phylogeny and substratepreference is also of great interest, with thephylogenetic affinities between guenon species stillunder debate. However, it is highly likely thatarboreal and terrestrial guenons are in two different

Am. J. Primatol.

Semi-Terrestriality of Cercopithecus Solatus / 11

clades and that positional behavior has played amajor role in guenon speciation events [Moulin et al.,2008; Perelman, 2011; Tosi et al., 2004; 2005a,b; Xinget al., 2007]. It is important to continue to analyzephylogenetic and morphological datasets from gue-non species, testing previous hypotheses and clarify-ing detailed points of difference [Gebo&Sargis, 1994;Manaster, 1979; Tosi et al., 2005a].

An interpretation of substrate preference adap-tations through time has been proposed by Gebo andSargis [1994], who analyzed guenon morphologywithin a phylogenetic framework. Based on themonophyly of several groups and of shared positionalbehaviors, these authors proposed hypotheticalarboreality for the ancestral guenon ancestor,followed by several (at least 6, depending on thesubstrate preference attribution of some species)independent adaptational events for terrestrialitythrough time. This scenario, however, is highlydependent on the base phylogeny used, namely themolecular phylogeny resulting from the electropho-retic study of 10 blood proteins proposed by Ruvolo[1988] and considered the “most accurate”. Morerecently, Sargis et al. [2008] proposed an alternativescenario based on work by both Ruvolo [1988] onblood proteins and Tosi et al. [2005a] on sexchromosome DNA. These results differed slightlyfrom one another, but the validity of the scenario wasconfirmed, suggesting one single adaptational eventfor terrestriality during guenon evolution. However,researchers have proposed other phylogenies overthe last two decades based on different characters,such as chromosome organization [Dutrillaux, 1988],mitochondrial DNA [Disotell & Raaum, 2002; Gu-schanski et al., 2013], nuclear DNA [Perelman et al.,2011], sex chromosomeDNA [Tosi et al., 2004; 2005b]or vocalizations [Gautier, 1988]. Topology congruen-cy is not always obvious and several scenarios remainpossible to explain species relationships. Guschanskiet al. [2013] noted great differences in topologybetween nuclear and mitochondrial results, whichcould be explained by a high rate of hybridization.However, most of these phylogenies agree with aseparation of arboreal and terrestrial species. Aclarification of the position of the sun-tailed monkeyis essential for the analysis of lifestyle and also ofguenon evolution.

The results of our study suggest semi-terres-triality for Cercopithecus solatus, as well as probablesemi-terrestriality for the Cercopithecus lhoestigroup. These results could affect the hypothesisproposed by Gebo and Sargis [1994] and Sargis et al.[2008]. We suggest, therefore, that the assumption ofarboreal ancestry still requires further consider-ation. In her PhD thesis, Terassin-Tholance [1995]proposed a semi-terrestrial ancestral condition withsome later terrestrial and arboreal adaptationalevents. As this hypothesis remains unpublished, ithas never really been evaluated by other researchers.

In Terrassin-Tholance’s theory, Erythrocebus patasandCercopithecus aethiops have undergone selectionsince the ancestral semi-terrestrial state, tendingtoward terrestrial species (she classified thesespecies as savanna semi-terrestrials). For Terrasin-Tholance, C. lhoesti, C. preussi and C. solatus alsoexpress a semi-terrestrial ancestral condition (sheclassified these species as forest semi-terrestrials).

Terrassin-Tholance’s hypothesis of a semi-ter-restrial ancestor is an intriguing alternative to theevolutionary models presented in previous studies.We tested this hypothesis by adding the substratepreference of each species to several of the previouslymentioned phylogenies. The semi-terrestrial ances-tor scenario is less parsimonious than the scenarioproposed by Gebo and Sargis [1994] and Sargis et al.[2008] if we use the phylogeny of Dutrillaux et al.[1988]. However, this scenario is more parsimoniousif we use the phylogenies of Ruvolo [1988] Tosi et al.[2005a] and Moulin et al. [2008] (Fig. 5). The semi-terrestrial ancestor scenario implies one adaptation-al event for terrestriality (forE. patas), two events forarboreality (Miopithecus talapoin and the arborealguenon group) and re-adaptation to semi-terrestrial-ity (possibly for C. neglectus and C. hamlyni),depending on phylogenies (Fig. 5). Tosi et al.[2004] proposed a single adaptational event forterrestriality in guenons but their conclusions aredifferent from ours as their approach is different.They distinguished the “arboreal” and “terrestrial”groups of guenons, considering them as two clades.Thus, they did not consider semi-terrestriality forguenons, since their approach was purely phyloge-netic, in contrast to our approach, which is bothbehavioral and functional. We are not able to test theancestral condition of the tribe Cercopithecini withour data.However, we believe that the possibility of asemi-terrestrial ancestor, proposed by Therassin-Tholance [1995], deserves further consideration. Itwould be interesting to evaluate the fit of empiricalresultswith this hypothesis vs the currently acceptedhypothesis of an arboreal ancestor for the group.

ACKNOWLEDGMENTSThe authors dedicate this contribution to the

memory of Annie Gautier-Hion, who died onJuly 13th 2011. As a primatologist and CNRSresearcher in ecology and ethology, she spent morethan 30 years studying African monkeys. “La Damede Paimpont”, as she was known, helped to set up aprimate center in France, based at the Paimpontbiological station.

We are greatly indebted to Jacques Cuisin, AnnePreviato and Julie Villemain of the LaboratoireMammif�eres et Oiseaux, Mus�eum national d’His-toire naturelle, Paris, who provided access to thecollections under their care. We also thank BrigitteSenut for her help in the interpretation of our results.

Am. J. Primatol.

12 / Motsch et al.

Advice provided by Elo€ıse Zoukouba is much appre-ciated by the authors. The authors would like tothank JessicaWhite for initial proof reading. Thanksalso to Pr. Eric Delson, Pr. Marina Cords, and a thirdanonymous reviewer, for their suggestions, whichgreatly improved the manuscript.

REFERENCESAltmann J 1974. Observational study of behaviour. Sampling

methods. Behaviour 49:227–266.Anapol F, Turner TR, Mott CS, Jolly CJ. 2005. Comparative

postcranial body shape and locomotion in Chlorocebusaethiops and Cercopithecus mitis. American Journal ofPhysical Anthropology 127:231–239.

Ankel-Simons F 2000. Primate anatomy an introduction. SanDiego: Academic Press. p. 506.

Badyaev AV, Young RL, OhKP, Addison C. 2008. Evolution ona local scale: developmental, functional, and genetic bases ofdivergence in bill form and associated changes in songstructure between adjacent habitats. Evolution 62:1951–1964.

Bello-Hellegouarch G, Potau JM, Arias-Martorell J, PastrorJF, P�erez-P�erez A. 2013. Brief communication: Morpho-logical effects of captivity: a geometric morphometricanalysis. American Journal of Physical Anthropology152:306–310.

Birkett LP, Newton-Fisher NE. 2011. How abnormal is thebehaviour of captive, zoo-living chimpanzees? PloS one 6:e20101 1–6.DOI: 10.1371/journal.pone.0020101.

Brugi�ere D, Gautier JP, Lahm S. 1998. Additional data on thedistribution of Cercopithecus (lhoesti) solatus. Folia Prima-tologica 69:331–336.

Burnaby TP 1966. Growth-invariant discriminant functionsand generalized distances. Biometrics 22:96–110.

Cardini A, Elton S. 2008. Does the skull carry a phylogeneticsignal? Evolution and modularity in the guenons. BiologicalJournal of the Linnean Society 93:813–834.

Christiansen P, StephenW. 2007. Bite forces and evolutionaryadaptations to feeding ecology in carnivores. Ecology88:347–358.

Claude J 2008. Morphometrics with R. Springer. 316. p.Clutton-Brock TH, Harvey PH. 1977. Primate ecology and

social organization. Journal of Zoology 183:1–39.Coward WM, Mc Conathy D. 1996. A Monte Carlo study of the

inferential properties of threemethods of shape comparison.American Journal of Physical Anthropology 99:369–377.

DelsonE, Terranova CJ, JungersWL, et al. 2000. Bodymass inCercopithecidae (Primates, Mammalia): Estimating andscaling in extinct and extant taxa. Anthropological Papers ofthe American Museum of Natural History 83:1–159.

Disotell T, Raaum R. 2004. Molecular timescale and gene treeincongruence in the guenons. In Glenn ME, Cords M,editors. The guenons: Diversity and adaptation in Africanmonkeys. New York: Kluwer Academic/Plenum Publishers.p 27-36.

Dutrillaux B 1988. Chromosome evolution in primates. FoliaPrimatologica. 50:134–135.

Escarguel G 2005. Mathematics and the lifeway of Mesopi-thecus. International Journal of Primatology 26:801–823.

Fleagle JG 1999. Primate adaptation and evolution. SecondEdition. London: Academic Press.p p. 596.

Fleagle JG, Simons EL. 1982. The humerus ofAegyptopithecuszeuxis: a primitive anthropoid. American Journal of Physi-cal Anthropology 59:175–193.

Friendly M, Fox J. 2013. Candisc: visualizing generalizedcanonical discriminant and canonical correlation analysis.R package version 0. 6–5.

Gautier JP 1985. Quelques caract�eristiques �ecologiques dusinge des marais: Allenopithecus nigroviridis Lang 1923.Revue d’�ecologie (la Terre et la Vie) 40:331–342.

Gautier JP 1988. In: Gautier-Hion A, Bourli�ere F, Gautier J,Kingdon J, editors. Interspecific affinities among guenons asdeduced from vocalizations. Cambridge: Cambridge Univer-sity Press. p 194-226.

Gautier JP,MoysanF, Feistner ATC, Loireau J-N, Cooper RW.1992. The distribution of Cercopithecus (lhoesti) solatus. Anendemic guenon of Gabon. Revue d’�ecologie 47:367–381.

Figure 5. Substrate preferences mapped on the phylogenies proposed in Moulin et al. [2008], Tosi et al. [2005a] and Ruvolo [1988]. Weconsidered the ancestral condition to be semi-terrestrial (A/T) with some species adaptations to terrestrial (T) or arboreal (A) positionalbehaviors. Note that this scenario is more parsimonious than considering the ancestral condition as arboreal.

Am. J. Primatol.

Semi-Terrestriality of Cercopithecus Solatus / 13

Gautier-Hion A 1988. In: Gautier-Hion A, Bourli�ere F, GautierJ, Kingdon J, editors. Polyspecific associations among forestguenons: ecological, behavioural and evolutionary aspects.Cambridge: Cambridge University Press. p 127-139.

Gautier-Hion A, Gautier J. 1974. Les associations polysp�eci-fiques du plateau de M’passa. Gabon. Folia Primatologica22:134–177.

Gebo DL, Chapman CA. 1995. Habitat, annual, and seasonaleffects on positional behavior in Red Colobus monkey.American Journal of Physical Anthropology 96:73–82.

Gebo DL, Sargis EJ. 1994. Terrestrial adaptations in thepostcranial skeletons of guenons. American Journal ofPhysical Anthropology 93:341–371.

Gonzalez-Kirchner J 1996. Notes on the habitat use by theRusset-eared guenon (Cercopithecus erythrotis Waterhouse1838) on Bioko island. Equatorial Guinea. Tropical Zoology9:297–304.

Grant BR,Grant PR. 1996. Cultural inheritance of song and itsrole in the evolution of Darwin’s finches. Evolution 50:2471–2487.

Groves CP 2000. In: Whitehead PF, Jolly CJ, editors. Thephylogeny of the Cercopithecoidae. Cambridge: CambridgeUniversity Press. p 77-98.

Groves CP 2006. Taxonomy and bioeography of the primates ofWestern Uganda. In: Newton-Fisher NE, Notman H,Paterson JD, Reynolds V, editors. Primates of WesternUganda. New York: Springer. p 3-20.

Grubb P, Butynski TM, Oates JF. et al. 2003. Assessment ofthe diversity of African primates. International Journal ofPrimatology 24:1301–1357.

Guschanski K, Krause J, Sawyer S. et al. 2013. Next-generation museomics disentangles one of the largestprimate radiations. Systematic Biology 62:539–554.

Harrison MJS 1988. A new species of guenon (genusCercopithecus) fromGabon. Journal of Zoology 215:561–575.

Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. 2005.Very high resolution interpolated climate surfaces for globalland areas. International Journal of Climatology 25:1965–1978.

Hosey GR 2005. How does the zoo environment affect thebehaviour of captive primates? Applied Animal BehaviourSciences 90:107–129.

Hurov JR 1987. Terrestrial locomotion and back anatomy invervets (Cercopithecus aethiops) and patas monkeys (Eryth-rocebus patas). American Journal of Primatology 13:297–311.

Isbell LA, Pruetz JD, Lewis M, Young TP. 1998. Locomotoractivity differences between sympatric patas monkeys(Erythrocebus patas) and vervet monkeys (Cercopithecusaethiops): implications for the evolution of long hindlimblength inHomo. American Journal of Physical Anthropology105:199–207.

Janis C 1982. Evolution of horns in ungulates: ecology andpaleoecology. Biological Reviews 57:261–318.

Jenkins FA, Jr. 1973. The functional anatomy and evolution ofthe mammalian humeroulnar articulation. American Jour-nal of Anatomy 137:281–298.

Jolly CJ 1965. Origins and specializations of the long-facedCercopithecoidea. University of London. 710. p.

Jolly CJ 1967. In: Vagtborg H, editor. The evolution of thebaboons. vol. Austin:University of TexasPress. 2: p 427-457.

Jolly CJ 1972. The classification and natural history ofTheropithecus (Simopithecus) (Andrews, 1916), Baboons ofthe African Plio-Pleistocene. Bulletin of the BritishMuseumof Natural History (Geology) 22:1–123.

Kaplin BA 2001. Ranging behavior of the two species ofguenons (Cercopithecus lhoesi and C. mitis doggetti) in theNyungwe forest reserve, Rwanda. International Journal ofPrimatology 22:521–548.

Kaplin BA, Moermond TC. 2000. Foraging ecology of themountain monkey (Cercopithecus l’hoesti): Implications for

its evolutionary history and use of disturbed forest.American Journal of Primatology 50:227–246.

Khan BN 2013. Impact of captivity on social behaviour ofchimpanzee (Pan troglodytes). The Journal of Animal andPlant Sciences 23:779–785.

Kay RF 1984. In: Rodman PS, Cant JGH, editors. On the use ofanatomical features to infer foraging behaviour in extinctPrimates. New York: Columbia University Press. p 21-53.

Larson SG, Stern JT. 1989. The use of supraspinatus in thequadrupedal locomotion of vervets (Cercopithecus aethiops):implications for interpretation of humeral morphology.American Journal of Physical Anthropology 79:369–377.

Manaster BJ 1979. Locomotor adaptations within the Cerco-pithecus genus: a multivariate approach. American Journalof Physical Anthropology 50:169–182.

Martin RD1990. Primate origins and evolution: a phylogeneticreconstruction. Princeton University Press. 820. p.

McGrawWS 1996. Cercopithecid locomotion, support use, andsupport availability in the Tai Forest, IvoryCoast. AmericanJournal of Physical Anthropology 100:507–522.

McGraw WS 2000. Positional behaviour of Cercopithecuspetaurista. International Journal of Primatology 21:157–182.

McGrawWS2004. In: GlennME,CordsM, editors. Diversity ofguenon positional behaviour. In: New York: KluwerAcademic/Plenum Publishers. p 113-131.

Motsch P, Le Flohic G, Leclercq J, Gonzalez J-P. 2011.Contribution �a la r�e-�evaluation de l'aire de r�epartition dusinge �a queue de soleil (Cercopithecus solatus). Revue deprimatologie 3. Online at http://primatologie.revues.org/604.

Moulin S, Gerbault-Seureau M, Dutrillaux B, Richard FA.2008. Phylogenomics of African guenons. ChromosomeResearch 16:783–799.

Napier JR, Napier PH. 1967. A handbook of living primates.Academic Press New York 546 p

Nogueira MR, Peracchi AL, Monteiro LR. 2009. Morphologicalcorrelates of bite force and diet in the skull and mandible ofphyllostomid bats. Functional Ecology 23:715–723.

NowakK, le RouxA, Richards SA, Scheijen CJP,Hill RA. 2014.Human observers impact habituated samango monkeys’perceived landscape of fear. Behavioral Ecology 1–6.

Oxnard CE 1963. Locomotor adaptations in the primateforelimb. Symposium of the Zoological Society of London10:165–182.

Peignot P, Fontaine B, Wickings EJ. 2000. Habitat exploita-tion, diet and some data on reproductive behaviour in asemi-free-ranging colony of Cercopithecus lhoesti solatus, aguenon species recently discovered in Gabon. Folia Prima-tologica 70:29–36.

Podos J 2001. Correlated evolution of morphology and vocalsignal structure in Darwin’s finches. Nature 409:185–188.

Prost JH 1965. A definitional system for the classification ofprimate locomotion. American Anthropologist 67:1198–1214.

Quris P 1976. Donn�ees comparatives sur la socio�ecologie dehuit esp�eces de Cercopithecidae vivant dans unememe zonede foret primitive p�eriodiquement inond�ee (nord-est duGabon). Revue d’�ecologie (la Terre et la Vie) 30:193–209.

R Core Team. 2013. R: A language and environment forstatistical computing. R foundation for statistical comput-ing, Vienna, Austria. URL http://www.R-project.org/.

Ripley S 1967. The leaping of langurs: a problem in the study oflocomotor adaptation. American Journal of Physical An-thropology 26:149–170.

Rodman PS 1979. Skeletal differentiation of Macaca fascicu-laris and Macaca nemestrina in relation to arboreal andterrestrial quadrupedalism. American Journal of PhysicalAnthropology 51:51–62.

Rose MD 1979. Positional behaviour in natural populations:some quantitative results of a field study of Colobus gereza

Am. J. Primatol.

14 / Motsch et al.

andCercopithecus aethiops. In:MorebeckME,PreuschoftH,Gomberg N, editors. Environment, behaviour, andmorphol-ogy. New York: Gustav Fisher. p 75–94.

Rose MD 1988. Another look at the anthropoid elbow. Journalof Human Evolution 17:193–224.

Ruff CB 2002. Long bone articular and diaphyseal structure inold world monkeys and apes. I: Locomotor effects. AmericanJournal of Physical Anthropology 119:305–342.

Ruvolo M 1988. In: Gautier-Hion A, Bourli�ere F, Gautier J,Kingdon J, editors. Genetic evolution in the Africanguenons. Cambridge: Cambridge University Press. p127-139.

Sargis EJ, Terranova CJ, Gebo DL. 2008. Evolutionarymorphology of the guenon postcranium and its taxonomicimplications. In Sargis EJ, Dagosto M, editors. Mammali-an evolutionary morphology. Dordrecht: Springer. p361-372.

Schultz AH 1969. The Life of Primates. London: Weidenfels &Nicholson. 383. p.

Senut B 1986. Long bones of the primate upper limb:Monomorphic or dimorphic?. Human Evolution 1:7–22.

Senut B 1991. Forme et mouvement chez des primatesn�eog�enes de l’ancien monde. Geobios 13:193–199.

Slice DE, Taylor AB. 2005. A geometric morphometricassessment of the relationship between scapular variationand locomotion in African apes. In: Slice DE, editor. ModernMorphometrics in Physical Anthropology. New York:Kluwer Academic/Plenum Publishers. p 299-318.

Smith RJ, Cheverud JM. 2002. Scaling of sexual dimorphismin body mass: A phylogenetic analysis of Rensch’s rule inPrimates. International Journal of Primatology 23:1095–1135.

Soligo C, Martin RD. 2006. Adaptive origins of primatesrevisited. Journal of Human Evolution 50:414–430.

Struhsaker TT 1981. Forest and primate conservation in EastAfrica. African Journal of Ecology 19:99–114.

Su DF, Jablonski NG. 2009. Locomotor behaviour and skeletalmorphology of the odd-nosed monkeys. Folia Primatologica80:189–219.

Terrassin-Tholance C 1995. De la terrestrialit�e �a l’arborico-lisme: anatomie fonctionnelle compar�ee de la ceinturescapulaire et du membre ant�erieur des Cercopith�eques.PhD Thesis. University of Rennes. 243. p.

Tosi AJ, Melnick DJ, Disotell TR. 2004. Sex chromosomephylogenetics indicate a single transition to terrestriality inthe guenons (tribe Cercopithecini). Journal of HumanEvolution 46:223–237.

Tosi AJ, Detwiler KM, Disotell TR. 2005a. X-chromosomalwindow into the evolutionary history of the guenons(Primates: Cercopithecini). Molecular Phylogenetics andEvolution 36:58–66.

Tosi AJ, Detwiler KM, Disotell TR. 2005b. Y-Chromosomalmarkers suitable for noninvasive studies of guenon hybrid-ization. International Journal of Primatology 26:685–696.

VenablesWN, Ripley BD. 2002.Modern applied statistics withS. Fourth edition. New York: Springer.

White LJT 1994. Patterns of fruit-fall phenology in the Lop�eReserve, Gabon. Journal of Tropical Ecology 10:289–312.

Wright KA 2007. The relationship between locomotor behav-iour and limb morphology in brown (Cebus apella) andweeper (Cebus olivaceus) capuchins. American Journal ofPrimatology 69:736–756.

Xing J, Wang H, Zhang Y. et al. 2007. A mobile element-basedevolutionary history of guenons (tribe Cercopithecini). BMCBiology 5:1–10.

Youlatos D 1999. Etude fonctionelle multivari�ee de l’astragaleet du calcan�eum de Mesopithecus pentelici, Wagner 1839(Cercopithecoidea , Primates). Primatologie 2:407–420.

Youlatos D 2003. Calcaneal features of the Greek Mioceneprimate Mesopithecus pentelicus (Cercopithecoidea: Colobi-nae). Geobios 36:229–239.

Youlatos D, Koufos GD. 2010. Locomotor evolution ofMesopithecus (Primates: Colobinae) from Greece: evidencefrom selected astragalar characters. Primates 51:23–35.

Youlatos D, Couette S, Koufos GD. 2012. A functionalmultivariate analysis ofMesopithecus (Primates: Colobinae)humeri from the Turolian of Greece. Journal of HumanEvolution. 63:219–230.

Am. J. Primatol.

Semi-Terrestriality of Cercopithecus Solatus / 15