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SHAPE MEETS FUNCTION:STRUCTURAL MODELS IN PRIMATOLOGY

Edited by Emiliano Bruner

Proceedings of the 20th Congress of the International Primatological Society

Torino, Italy, 22-28 August 2004

MORPHOLOGY AND MORPHOMETRICS

Introduction

The genera Alouatta, Ateles, Brachyteles, andLagothrix, are the living representatives of thefamily Atelidae Gray 1825, forming a mono-phyletic taxon. Extant howlers are grouped intothe Mycetinae subfamily, which includes the fos-sil genus Stirtonia (Szalay & Delson, 1979) andpossibly the subfossil genus Paralouatta (Rivero& Arredondo, 1991; but see Horovitz &McPhee, 1999). Extant howler monkeys (genusAlouatta) represent one of the most distinctivetaxa of the Neotropical primatological fauna.

The genus Alouatta includes about 10 speciesand up to 19 subspecies distributed betweenMexico and Argentina (see Groves, 2001). Theyare generally divided into a palliata group (main-ly Central America) and a seniculus group (SouthAmerica, including A. caraya). Despite the con-troversies on the phylogenetic relationships with-in the subfamily Atelinae, there is a generalagreement about the phyletic independence ofAlouatta with respect to all the other genera(Rosenberg, 1981; Horovitz & Mayer, 1995;Schneider et al., 1996). According to a mt-DNAanalysis, the two subfamilies show a divergence

JASsJournal of Anthropological Sciences

Vol. 82 (2004), pp. 47-66

A geometric morphometric approach to airorhynchy andfunctional cranial morphology in Alouatta (Atelidae,Primates)

Emiliano Bruner1,2, Simone Mantini1 & Giorgio Manzi1,2

1) Dipartimento di Biologia Animale e dell’Uomo, Università La Sapienza, Piazzale Aldo Moro 5, 00185Roma. e-mail: [email protected]

2) Istituto Italiano di Paleontologia Umana, Piazza Mincio 2, 00198 Roma

Summary – The skull of the howler monkeys (Alouatta spp., Atelidae) is characterised by a generalisedrotation of the splanchnocranium with respect to the neurocranial antero-posterior axis. This process,referred to as airorhynchy, is the result of a derived structural relationship between basicranium, vault, andfacial districts. A number of variables – such as diet and social behaviour – probably co-evolved with theremodelling of the cranial functional matrix. We used a landmark-based analysis to explore the geometri-cal model of the skull in the genus Alouatta. Shape comparisons were performed by using superimpositionprocedures and the Euclidean distance matrix. In the latter analysis, a method is proposed in order to visu-alise variations of form through chromatic maps and interpolant functions. The comparison with other gen-era of Atelidae shows a marked neurocranial flattening in Alouatta as well as muzzle projection andenlargement, nuchal flattening, relative basicranial lengthening, and tilting of the occipital foramen. Onlyminor differences were visible in relation to facial shape, suggesting that significant changes depend on therelationship between splanchnocranium and neurocranium, rather than on localised anatomical variations.The limited vault development constrained by the basicranial structures probably involved the extremeretroflexion of the basal angle. Airorhynchy can be interpreted as an additional adjustment to fit this struc-tural network beyond the biomechanical range of the cranial base hypoflexion. This cranial functionalmatrix is directly related to feeding and social changes, representing an interesting evolutionary “package”.In Pongo pygmaeus a similar process is associated with a different structural pattern, mostly related to theflattening of the upper facial structures, maxillary midsagittal enlargement, and palatal tilting.

Keywords – Alouatta, functional craniology, airorhynchy, Pongo, geometric morphometrics, Euclideandistance matrix analysis.

time close to 16 million years before present(Ma), while the Trans-Andean and Cis-AndeanAlouatta groups may diverged about 7 Ma(Cortés-Ortiz et al., 2002). The evolutionarypatterns are not as clear, because of the mosaicvariability expressed in the atelids, which proba-bly includes a large percentage of plesiomorphiccharacters as well as parallelisms and homoplasticfeatures. Alouatta and Brachyteles share manydental traits because of the comparable size-relat-ed dietary specialisation. Alouatta and Lagothrixshare many postcranial traits, which were influ-enced by the locomotion patterns (see Szalay &Delson, 1979), and probably some plesiomor-phic features like the enlarged zygomatico-facialeforamen displayed by the Oligocenic fossil genusParapithecus (Simons, 2004) and occasionally byAotus (quoted in Osman Hill, 1962: p. 22).

Alouatta displays a set of rather interestingfeatures when compared to the other Atelids,leading early authors to describe this taxon as“the most derived [genus] of the recent Cebidae”,“unmistakable … on account of its peculiarform”, and with a “bestial appearance” (seeOsman Hill, 1962). A trichromatic visionevolved in howlers independently from thecatarrhine evolution (see Jacobs, 2004; Heesyand Ross, 2004). The cranial anatomy is veryspecialised. The hyoid bone is extremely devel-oped, forming large vocal sacs (Schön, 1971)that strongly characterise the howlers communi-cation system accounting for the intense loudcalls produced by isolated or grouped individu-als. The cranial structure is rather different fromthe basic morphology of the extant platyrrhini,because of the extreme airorhynchy. Airorhynchycan be defined as a dorsoventral rotation of max-illary structures, or the upward rotation ofsplanchnocranial functional axis onto the neuro-cranial one. As a consequence of to the subse-quent separation between face and braincase, themandibular ramus enlarges to fill the structuralgap between the occlusal plane and themandibular articulation. In Alouatta, theenlargement of the ramus is associated with thedevelopment of the masseter, and the develop-ment of the hyoid bone. The former morpholo-gy is associated with a folivourous diet, while the

latter is associated with the social structure of thehowlers. Although the development of themandible was hypothesised to have the principalrole within this structural network (Osman Hill,1962), it is not possible to split its causes andconsequences in an evolutionary perspective, asthese processes depend on a general rearrange-ment of the whole functional matrix of the skull.

Interestingly, airorhynchy has also beendescribed in Pongo pygmaeus, associated –- as inAlouatta – with the enlargement of the masseterand the development of vocal sacs (Shea, 1985).Alouatta also shares some morphological affini-ties with the cranium of the Oligocene fossilgenus Aegyptopithecus, mostly in the frontal areas(Simons, 1987). It has also been hypothesisedthat the two genera share a similar body size andlocomotory system (see Rasmussen, 2002). Acomparison between Alouatta and Aegyptopithecuscould thus be useful to suggest comments on theevolutionary history of the howlers’ morphology.

Although Alouatta represents a unique andextremely specialised taxon within the evolution-ary radiation of extant primates, the literature onits morphology and anatomy is rather scarce andmostly based on general anatomical descriptions.This explorative analysis is aimed at creating abasic framework for future investigations on thisgenus, through a “geometric dissection” of itscranial morphology. Different superimpositionprocedures were used to compare the cranialshape in Alouatta with the skull of the otheratelids. The process of airorhynchy in this mor-photype was also compared with the analogouschanges described in Pongo, in order to considerdifferences and affinities between these two line-ages. Finally, we performed a comparison withthe cranial shape in Aegyptopithecus in order topropose some general considerations on the evo-lution of the Mycetinae cranial anatomy.

Materials and methods

SampleIn this explorative analysis, Euclidean three-

dimensional coordinates were sampled fromeight adult Alouatta belonging to the seniculusgroup, and averaged in order to compute a mean

48 Alouatta skull morphology

configuration of landmarks. Only one adultspecimen represents each of the other atelidsgenus. Unfortunately, the rear vault of the onlyLagothrix presently available is damaged, andonly the facial structures were compared. OneCebus was included as non-Atelids morphologi-cal outgroup, as well as a cast of the 1966 com-plete skull of Aegyptopithecus (see Rasmussen,2002). We also considered one adult male Pongoand one adult male Pan in order to compare theairorhynchy in howlers and orangs. Althoughthis descriptive analysis cannot check the within-genus and between-sexes variability, it is assumedthat the intergeneric differences should be largerto allow a generic and explorative morphologicalcomparison. Data were sampled at the Museumof Anthropology Giuseppe Sergi, in Rome(Bruner & Manzi, 2001).

Shape comparisonWe used landmark coordinates and superim-

position to compare the cranial geometry in dif-ferent taxa, both in two and three dimensions. Athree-dimensional bilateral configuration of 42landmarks was selected to describe the cranialmorphology (Tab. 1; Fig. 1). The entire skull wasconsidered, as well as a sub-configuration includ-ing only the facial morphology. Landmarks weresampled with a Microscribe 3DX (ImmersionCorporation). Using the three-dimensionaldataset, two-dimensional data were computed

with MORPHEUS ET AL. (Slice, 2000) by align-ment of the whole sample according to thePrincipal Component eigenvectors, and subse-quently projecting the resulting coordinates on alateral plane (only the left side was used in theshape comparisons). The coordinate systemswere superimposed by Procrustes (both 3D and2D data) and Bookstein Superimposition (2Ddata) using MORPHEUS ET AL. (Slice, 2000), andshape differences were visualised using geometri-cal comparison and thin-plate spline (Bookstein,1991). The first procedure operates a translationof the coordinate systems to a common centroid,scaling to unitary centroid size, and a rotationbetween corresponding landmarks using a least-squares approach. The second procedure super-imposes the configuration onto a common base-line. Bookstein superimposition was used tocompare 2D configurations relatively to theneurocranial length (nasion-opisthocranion).The information available from these twosuperimpositions is rather complementary:while the first normalises the effect of size dif-ferences (i.e. approaching “shape”) the second isuseful to compare phenotypic variations withrespect to a specific functional/structural refer-ence (the neurocranial axis).

Procrustes distances were computed byTPSSMALL 1.19 (Rohlf, 1998) and visualisedaccording to the unweighted pair-group methodusing arithmetic averages (UPGMA) cluster pro-

Fig. 1 - Complete three-dimensional configuration of landmarks (42), shown in lateral view(basicranial landmarks are not visible). Landmarks are plotted on the skull of Alouatta(a) and linked to produce a geometric reference model (b). See Table 1 for landmarksdescription.

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cedure by SYNTAX 2000 (Podani, 1997), in orderto check the main phenotypic affinities.

Euclidean Distance Matrix Analysis(EDMA) was used to perform a further compar-ison, in order to check form differences regard-less of scaling procedures (see Richtsmeier et al.,2002). A subset of 17 lateral-projected land-marks was used to limit the number of inter-landmark distances. EDMA were performedusing WINEDMA (Cole 2002). Interlandmarkdistances exceeding 2 standard deviations fromthe mean value of the whole Form DifferenceMatrix (FDM) were considered as determinantinterlandmark distances. Landmarks with a medi-an distance value exceeding 5% of the averagemedian value were considered as influential land-marks. The median variation of each landmarkfrom the FDM was used to compute and map aninterpolating function in order to visualise thepattern of form differences (Form DifferenceMaps). Maps were computed by SURFER 7.0(Golden Software, Inc.), using a radial basisfunction through multiquadric interpolation(Carlson & Foley, 1991), suggested for smallsamples and scattered data. Interpolations withother common functions gave overall similarresults. These maps allow a visualisation of theform differences, describing patterns of increas-ing/decreasing interlandmark distances. Theminimum represents areas of relative shortening,and the maximum value represents areas of rela-tive lengthening. The intermediate value repre-sents a mean size difference between the twoforms, expressed as a ratio between each inter-landmark value (ratio = 1 means no difference).

Anatomical notes on the cranial structure of theAtelids

The configuration used in this explorativeanalysis is based almost entirely on type I land-marks (Bookstein, 1991), according to the bio-logical principle of homology. In general, in geo-metric morphometrics the operational homologyconcept can offer a more useful reference (Smith,1990), in considering the structural parametersof the anatomical system. The inter-specific vari-ability often makes it difficult to rely on homol-

ogy, and this is the case with the atelids skull(Fig. 2). The inter-orbital area represents a veryimportant source of information, because of itsrole in convergence, encephalisation, and in therelationship between face and vault. Landmarksfrom this district were not included in the pres-ent study, because of the lack of correspondencebetween the different taxa. Usually, the maxillaryprocesses reach the frontal suture separating theipsilateral nasal and lacrimal bones. This patternallows the recognition of two osteometric points,namely maxillofrontale and dacryon (see White &Folkens, 2000). This is also the pattern found inCebus. In Lagothrix, the maxillary processes meetabove the nasal bones, whose lateral borders con-verge at nasion, while the two maxillofrontaleconverge toward the midsagittal plane.Brachyteles shows a marked superior thinning ofthe maxillary processes, and a tendency to over-lap dacryon with maxillofrontale. In Ateles themaxillary processes do not reach the frontalsuture, being separated by the lacrimal bones.Alouatta displays a pattern similar to Ateles, withan almost constant lacrimo-nasal suture that,however, is limited in young specimens (Osman-Hill, 1962). Furthermore, the nasal bones areextremely different in the four genera: broad andshort in Lagothrix, curved and convergingupward in Brachyteles, thin and converging inAteles, and almost parallel in Alouatta. Otherfunctional areas such as the temporal fossa(Bruner et al., nd) display a similar conditionamong the Atelids skull. Clearly, further studiesare needed to describe the intra-generic andintra-specific variability of these features. It isworth noting the difficulties in considering bio-logical homology in these variable structures.Future analyses must be necessary developed soas to carefully consider the biological correspon-dence.

Results

Three-dimensional shape comparisonsFigure 3 shows the skull shape 3D compar-

isons between the Alouatta morphology and theother genera considered. In Alouatta there is a

clear midsagittal enlargement of the premaxillarystructures and lower face, with Brachyteles alsoshowing a more depressed nasal area comparedto the other specimens. The maxillary complexwidens (mostly when compared with Ateles)except when compared with Brachyteles. Amarked frontal bone flattening is associatedwith a loss of frontation, i.e. a marked inclina-tion of the orbital surface. Orbits are also rela-tively narrower. This configuration of the upperface is extreme when compared to the Cebusmorphology. The cranial base of Alouatta islengthened, because of the backward shifting ofthe spheno-occipital suture. In Cebus, the baseis further shortened because of the backwardposition of the posterior palatal spine. The vaultin Alouatta is extremely flattened, with thebregma in a relatively forward position. Theneurocranium is relatively narrow, mostly com-

pared to Ateles, which in contrast has narrowerzygomatic arches. Malar bones are relativelywidened only in Cebus. The whole nuchal planeis rotated upward, and the foramen magnum isconsequently tilted backward.

The differences are less marked in consider-ing the superimposition of the facial shape (Fig.4). Alouatta shows a light premaxillar enlarge-ment and upper facial flattening. The midface isalso depressed, except when compared withBrachyteles that displays an even more flattenedprofile. The maxilla is relatively narrower inAteles and wider in Cebus. The orbital surfaces areno longer inclined, and the frontation is alsoimproved because of a backward shifting of the infe-rior orbitale with respect to the muzzle area. Orbitsare narrower, particularly in comparison to Atelesand Brachyteles. Because of the maxillary develop-ment, malars are relatively shifted backwards.

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Tab. 1 - Landmarks and definitions.

When the overall phenotypic affinity is con-sidered as Procrustes distances, the skull ofAlouatta differs from the other Atelids (Fig. 5a)more than Cebus. In contrast, the facial shape ishighly comparable with the Brachyteles and Atelesconfigurations (Fig. 5b).

Two-dimensional shape comparisonsIn figure 6 the pairwise comparisons between

the skull shapes are computed on the 2D pro-jected data (lateral projection, left side). TheProcrustes superimposition shows the maxillaryenlargement and premaxillary projection inAlouatta, and the midfacial flattening in

Brachyteles. Orbits are more verticalised in Cebus.In Alouatta the entire vault (including the frontaland orbital areas) is extremely flattened, thenuchal structures are tilted backward andupward, and the cranial base (posterior palatalspine to spheno-occipital suture) is lengthened.The malar area varies in each species. Brachytelesshows the least amount of shape differences com-pared to Alouatta. The distortion grids stress theneurocranial flattening, nuchal rotation, muzzleenlargement, and basicranial lengthening.Compared to Cebus, Alouatta shows a verticalfacial compression related to the premaxillaryrotation, and a coronal structural compression at


Fig. 2 - The interorbital area in the atelids. Alouatta and Ateles show a contact between lacrimal andnasal bones. In Brachyteles the contact between the maxillary processes and the frontalbone is almost limited to a single point. In Lagothrix, the maxillary processes meet abovethe nasal bones, forming a intermaxillary suture. Labels: m: maxilla; n: nasal bone; l:lacrimal bone; f: frontal bone.

53E. Bruner et al.

Fig. 3 - Pairwise comparisons of the complete configurations of landmarks after Procrustes super-imposition (left lateral and superior views).


the level of the porion. Compared to Ateles, theface is rotated on the neurocranial axis but notvertically compressed. The coronal structuralcompression is localised at the level of the pteri-on, and the maxilla is significantly enlarged.Compared to Brachyteles, there is a marked mid-facial enlargement, and a minor structural com-pression at the level of the porion. In all cases theflexion of the neurocranial structures onto thefacial one is well expressed.

Through the baseline superimposition, it ispossible to compare shapes in relation to thesame neurocranial length. Brachyteles is moresimilar to Alouatta than the other two taxa. Thedifferences concern the upper and midfacialenlargement and neurocranial flattening. Atelesand more specifically Cebus show a furtherreduction of splanchnocranium and verticalisa-tion of the orbits. Interestingly, by superimpos-

ing the neurocranial axis, the orientation of theforamen magnum shows a very limited rota-tion. It is worth noting that while theProcrustes superimposition better describes theoverall phenetic affinity, the Bookstein super-imposition is suitable to promote structuralhypotheses (when the baseline is assumed to rep-resent a functional reference).

Pongo vs PanFollowing the Procrustes superimposition,

the main differences identified between the Panand Pongo cranial shapes (Fig. 7) concern amarked frontal flattening and maxillary enlarge-ment in the latter. The maxilla-premaxilla com-plex undergoes a sagittal development withoutwidening, showing a relative inclination of thealveolar border. The orbits are smaller, but thereis no loss of frontation. The neurocranium

Fig. 4 - Pairwise comparisons of the facial configurations of landmarks after Procrustes superimpo-sition (left lateral view).

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widens posteriorly, and the nuchal area becomesshorter and taller. The foramen magnum isslightly tilted backwards. The zygomatic archesenlarge. The cranial base does not lengthen, andthe vault does not flatten except at the level ofthe frontal squama.

Comparing the projected two-dimensionalcranial shapes in Pongo and Pan in lateral view byProcrustes superimposition, the former shows amarked frontal flattening with only a minor rel-ative vertical shortening of the vault. In contrastthe nuchal area is relatively taller. The develop-ment of the maxilla-premaxilla complex is asso-ciated to a rotation of the alveolar border, with-out changes in the orientation of the lower andmidfacial profile. The cranial base is scarcelylengthened, and the foramen magnum is rathertilted backward without a posterior displace-ment. There is a strong forward shifting of theinferior border of the zygomatic arch, but themalar/pteric areas are quite comparable. There isno clear loss of frontation. The distortion gridsare mainly characterised by the zygomatic shift-ing and by the neurocranial tilting associated tothe vault and frontal flattening, and nuchalenlargement.

The neurocranial superimposition emphasis-es the neurocranial/basicranial vertical develop-ment in Pongo mainly in relation to the lowerareas, and the forward enlargement of the middleand lower face associated to the zygomatic move-ment. There is a palatal tilting and loss of fronta-tion, without rotation or displacement of theforamen magnum.

Euclidean Distance Matrix AnalysisThe Euclidean distance matrix comparison

was computed between Alouatta and Brachytelesand between Pongo and Pan, to compare the sim-ilar airorhynchy patterns. Alouatta/Brachyteles - The FDM shows a similarsize for the two specimens (mean and standarddeviation for all the interlandmark distances:0.99 ± 0.13). The influential landmarks show alengthening at the rhinion (median ratio = 1.10),and shortening at superior orbital rim (0.94),opisthocranion (0.95), and bregma (0.87). Thedeterminant interlandmark distances show ashift of the rhinion from the inferior orbital rim(ratio = 1.73) and a shortening of the distancebetween porion and the spheno-occipital suture(0.68). Furthermore, there is a general involve-

Fig. 5 - UPGMA phenograms computed on the Procrustes distances, considering the complete(a) and facial (b) configurations (Alo: Alouatta; Ate: Ateles; Bra: Brachyteles; Ceb:Cebus; Lag: Lagothrix).


ment of landmarks in relation to vault andnuchal flattening. The map of the form differ-ence interpolation stresses the flattening of theneurocranium and the muzzle forward develop-ment (Fig. 8a).Pongo/Pan - The FDM shows a larger size forPongo (1.14 ± 0.17). The influential landmarksshow a relative lengthening at the prosthion(median ratio = 1.21), premolar (1.26) and

molar (1.23) areas, and basion (1.21), with rela-tive shortening at the orbital rim (1.01-1.06),nasion (1.00), and bregma (1.07). The determi-nant interlandmark distances again show a shiftof the rhinion from the inferior orbital rim (ratio= 2.10), and a relative approaching between thelateral orbital border and nasion (0.65). There isa general involvement of landmarks related tonuchal, vault, and frontal flattening. The map of

Fig. 6 - Pairwise comparisons of the complete configuration of landmarks after two-dimension-al lateral projection (26 landmarks). Comparisons are visualised by Procrustes super-imposition of the geometrical model (left), distortion grids and thin-plate spline (mid-dle), and baseline superimposition on the neurocranial length (right).

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the form difference interpolation stresses a short-ening of the supraorbital landmarks and thedownward enlargement of the maxilla (Fig. 8b).Aegyptopithecus

Only some landmarks are available on theAegyptopithecus cast, mostly because of thepreservation of the specimen. Comparing theAlouatta and Aegyptopithecus cranial shape bysuperimposition, a structural affinity is easilyrecognised mostly because of the muzzleenlargement and because of the similar rela-tionship between facial and neurocranial dis-tricts (Fig. 9). The maxillary complex is moredeveloped in the Oligocenic taxon, even thoughit is relatively narrower compared to Alouatta.The neurocranium shows similar proportions.The most important difference is observed atthe foramen magnum: in both cases it is placedin a posterior position, but in Aegyptopithecus isnot tilted as in the howler. The distortion gridfrom the lateral projection stresses the relativesplanchnocranial development and the absenceof a clear inclination of the occipital foramen inthe former.

Discussion

In view of the explorative nature of theseresults, some comments are provided on thestructural craniology in Alouatta, on the phylo-genetic patterns of the Atelids, and on the paral-lel evolution of airorhynchy in Pongo pygmaeus.

Cranial structure and evolution in AlouattaThe shape comparisons between the Atelids

genera provide a general description of the struc-ture of the skull in Alouatta. The entire neuro-cranium is extremely flattened, and at the sametime narrower than that of the other atelids. It isnoteworthy that Alouatta shows an early cessa-tion of neurocranial growth related to an earlyobliteration of all the cranial sutures (quoted inOsman Hill, 1962: p.16), and it is clear that thetiming of craniosynostosis had a major role inthe evolution of the cranial morphology in thismorphotype. The flattening of the frontal boneis associated to a relative posterior shortening ofthe frontal squama and inclination of the orbits.The subsequent orbital morphology characteris-es Alouatta as probably the least frontatedanthropoid (Bruner et al., 2002). It is interestingto note that orbits are inclined with respect tothe neurocranial axis, but not considering thefacial morphology alone. The morphogeneticprocesses leading to a generalised flattening ofthe neurocranial and basicranial structures occuralmost entirely during the post-natal growth,with the early ontogenetic stages showing a moretypical basikyphosis that is partially preserved inadults along the brainstem (Osman Hill, 1962).Anyway, Jeffery described interesting differencesbetween Alouatta and Macaca during prenatalontogeny (Jeffery, 2003). In both species the bas-icranial retroflexion (i.e. hypoflexion) is correlat-ed with brain growth and development, but in

Fig. 7 - Pairwise comparison between Pan and Pongo after Procrustes superimposition (left lat-eral and superior views).


Fig. 8 - Form Difference Maps comparing Alouatta versus Brachyteles (a) and Pongo versus Pan(b). The configuration is based on 17 lateral-projected landmarks. The median valuesfrom the Form Difference Matrix of each landmark are interpolated using a multiquadricradial basis function (other similar functions do not change the overall pattern). Thescale provides a quantification of the processes, referring to the median ratio betweenthe interlandmark distances of the numerator and that of the denominator. In Alouatta,a vault vertical flattening associated to a forward muzzle development is observed,while in Pongo there is a supraorbital backward flattening associated to a downwardpremaxilla/maxilla development.

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Fig. 9 - Pairwise comparisons between Alouatta and Aegyptopithecus through Procrustessuperimposition of two-dimensional left lateral projections.

Alouatta this process is faster, associated withlower rates of total and posterior cranial baselenghtening, and associated with the infratentor-ial absolute and relative development.Furthermore, in Alouatta the volumetric brainexpansion is generally slower, but the cranial baseangle is always much higher than in macaques ofsimilar maturation quotient, and the infratento-rial (i.e. cerebellar) structures are relatively moredeveloped (see details in Jeffery, 2003). All thesefeatures must be involved in the final neurocra-nial morphology of the howler monkeys, andshould be carefully considered in terms of struc-tural correlations between cranial parts. Thefaster retroflexion stresses neurocranial flatteningand airorhynchy, which seem to be anyway evi-dent since the earliest fetal stages (at least at the40% of the total prenatal period). The scarcelenghtening of the clivus is probably involved inthe basioccipital shortening and nuchal rotation,also necessarily affected by the structural adjuste-ments related to the infratentorial development.The slower rate of cerebral growth leads to a gen-eralised neurocranial limited enlargement.

The basicranium flattens and lengthensthrough the stretching of the sphenoid body, dis-placing the spheno-occipital suture and the fora-men magnum backward. The pneumatisation ofthe sphenoidal body in Alouatta (Osman Hill,1962) is probably secondarily related to thissagittal development between the vomer and thespheno-occipital suture.

Considering the importance of the basicrani-um and in particular of the spheno-occipitalsuture in the development of the cranial func-tional matrix (e.g. Lieberman et al., 2000), thisprocess has probably a major role within the evo-lutionary changes described in Alouatta.Actually, the pressure along the anterior cranialbase can easily involve the rotation of thesplanchnocranium and be related to the flatten-ing of the vault. Ross et al. (2004) have recentlypublished an extensive analysis on the basicranialflexion in Primates. Species-specific averageddata from Ceboidea and Cercopithecoideashown the outstanding position of Alouattabecause of its basicranial length, cranial capacity,and cranial base angle. The basicranium is verylengthened when compared with the small cra-nial capacity (approximately 50 cc.), probablywith a large contribution of its anterior parts(Fig. 10a). Consequently, the encephalisationindex relative to the basicranial length isextremely small. The spatial packing hypothesisstates that in primates an increase in the relativeencephalisation index is associated with a flexionof the cranial base (see Ross et al., 2004).Alouatta does not fit the relationship describedfor the Ceboidea-Cercopithecoidea variation,showing even a less flexed base compared with itslow relative encephalisation or, conversely, asmall encephalisation index for such cranial baseangle (Fig. 10b). Some structural constraintsmust be involved in this configuration, where the


vault flattening and sphenoid lengthening actdirectly onto the cranial base flexion andendocranial volume. The howler’s base angle istheoretically compatible with a larger encephali-sation index, within the Ceboidea-Cercopithecoidea variation. In contrast, thescarce encephalisation index would require anextreme retroflexion of the base, probably out ofthe available structural range. It is therefore pos-sible to hypothesise that this extremely lowencephalisation index has involved the maxi-mum possible retroflexion, plus an additionalcompensatory adjustment represented by therotation of the splanchnocranium (namely,airorhynchy). The low encephalisation indexmust be related more to neurocranial flatteningand narrowing (i.e. scarce cranial capacity, relat-ed to slow rate of cerebral growth, suture fusion,etc.) than to an actual and absolute lengtheningof the sphenoid. The Euclidean Distance MatrixAnalysis (based onto the ratios between absolutevalues) largely supports this hypothesis, stressingthe neurocranial flattening and midface enlarge-ment, without any localised changes at the cra-nial base (see Fig. 8).

The same process tilts the occipital foramenbackwards, promoting a flattening of the nuchalarea and characterising the in vivo posture of thehowlers. It is worth noting that the foramenmagnum is much less inclined with respect to theneurocranial axis.

The premaxilla-maxilla complex undergoes arelevant development, through a general enlarge-ment and forward projection of the midface.

All these features increase the airorhynchy,producing a widening of theneurocranial/splanchnocranial axis and a mor-phological “crease” (Bookstein, 2000) betweenpterion and porion, which suggests that thesesurfaces may have a major structural role. Therelative position of the occipital foramen ontothe neurocranial length and the relative positionof the orbits onto the facial morphology stressthe hypothesis of different relationships betweenfunctional parts (face, base, and vault) withoutmajor local rearrangements. The peculiar mor-phology of the skull in Alouatta is actually rather“atelid-like” when the facial shape is considered

alone. Brachyteles shows an interesting phenotyp-ic similarity with Alouatta, despite a species-spe-cific flattening of the midfacial areas. In addi-tion, the shared interorbital anatomy betweenAlouatta and Ateles should be further explored.

These results and the comparison withAegyptopithecus can suggest some comments onthe evolution of the howlers’ cranial morphology.In the latter, the splanchnocranium is tilted ontothe neurocranial axis because of the scarce cranialdevelopment and the marked maxilla/premaxillarelative enlargement. The similar morphologydisplayed by Aegyptopithecus and Alouatta isprobably related to a similar relationshipbetween face and neurocranium, but there is noevidence of shared structural processes. Theantero-posterior muzzle enlargement in the spec-imen of the Oligocene is not associated with ageneral maxillary widening, and the foramenmagnum - although shifted to a posterior posi-tion - is not tilted as in Alouatta. In consideringthe muzzle shortening described along theanthropoids evolution and the peculiar nuchalshape in Alouatta, it is reasonable to hypothesisea parallelism between a derived condition in thehowlers and a plesiomorphic morphology forAegyptopithecus. In the latter, the skull morphol-ogy can be easily interpreted as an archaic expres-sion of the volumetric ratio between neurocrani-um and splanchnocranium. In Alouatta, the dif-ferent relationship between muzzle and cranialbase (sphenoidal lengthening and associatedshifting of the foramen magnum) suggests thatthe rotation of the facial axis is probably relatedto a secondary (i.e. derived) splanchnocranialenlargement associated to with a specific adap-tive context (Osman-Hill, 1962).

These inferences do not involve commentson the ancestral morphology of the Atelids them-selves, and on the within-group polarity of theircharacters, including airorhynchy. The probablephyletic relationships within the Atelids(Horovitz & Mayer, 1995) is largely charac-terised by mosaic patterns and a certain amountof homoplasy, as can be possibly hypothesisedcomparing postcranial and dental traits (Szalay& Delson, 1979). Furthermore, the fossil recordis rather scattered (Hartwig & Meldrum, 2002;

61E. Bruner et al.

Fig. 10 - Relationship between brain volume (BV; in cubic centimeters), basicranial length (BL: fora-men caecum - sella - basion; in centimeters), cranial base angle (CBA; degree), and indexof relative encephalisation (IRE; cube root of endocranial volume/BL), in Ceboidea (whitecircles), Cercopithecoidea (black circles), and Alouatta (A. belzebul, A. palliata; crosses).Data from Ross et al., 2004 (IRE = IRE5; BL = BL2; CBA = CBA4).


MacPhee and Horovitz, 2002) and the groupseems scarcely derived with respect to theOligocene primates, in relation to size, habits,and locomotion (Conroy, 1990). All these con-siderations suggest that their interesting evolu-tionary history is far from being understood.

Airorhynchy in Alouatta and PongoCompared to Pan, Pongo is mainly charac-

terised by a lower splanchnocranial enlargement,braincase vertical stretching, and supraorbitalflattening. The flattening at the supraorbitalstructures is very stressed, involving loss offrontation with respect to the neurocranial axisbut not in relation to the entire skull shape. Aminor upper vault flattening is associated with arelevant vertical stretching of the braincase. Thenuchal area undergoes a subsequent flatteningand relative widening. The foramen magnum isslightly tilted, but not displaced backwards.Interestingly, once more the occipital foramen isangled compared to the whole skull shape, butnot considering the neurocranial axis. Similarly,the cranial base does not show a marked length-ening. The premaxilla-maxilla complex shows asagittal development, mainly in relation to adownward shifting and inclination of the alveo-lar border. The zygomatic arches are veryenlarged and flared. It must be noted that oncemore the polarity of the structural condition inchimps and orangs has not been discussed, most-ly taking into account the phenotypic affinitybetween Pongo and the extinct Dryopithecinae.

In Pongo, Shea (1985) hypothesised thatairorhynchy can be associated to simognathism,supraorbital flattening, orbital shape, mandibleenlargement, nasal floor and ethmoid structure,and morphology of the anterior cranial fossa.According to both superimposition andEuclidean distance matrix analysis, there is noevidence of a clear midfacial flattening. Thelower and middle facial profile in Pongo seemsnot to differ from the shape expressed in Pan,except for a generalised enlargement. Rhinionshows even a further projection considering theoverall size increase in Pongo. The actual flatten-ing involves the upper face, including the nasion.

On the contrary, in comparing Pan and

Pongo, it was also hypothesised that the orbitalmorphology is independent upon airorhynchy,which was associated to palatal tilting and devel-opment of the temporal muscle (Penin & Baylac,1999). The comparison between Pan and Pongoshows different superimposition results in thepresent analysis and the work published by Penin& Baylac (compare Figure 2a in Penin & Baylac,1999). In both studies there is a frontal andnuchal flattening associated with a palatal tilting.In contrast, Penin & Baylac found a maxillaryrotation and relative neurocranial flattening.These differences can be related to the differentlandmarks considered, or to the use of unilateralvs. bilateral configurations. Anyway, these differ-ences once more stress the need of caution whenconsidering superimposed forms (Richtsmeier etal., 2002), suggesting a complementary use ofmultiple techniques. Different superimpositionsmust be compared, and integrated using coordi-nate-free approaches to “Form” such as theEuclidean Distance Matrix Analysis. This analy-sis is extremely useful to describe the actual geo-metrical differences between systems of coordi-nates, even if results are more difficult to display(Cole & Richtsmeier, 1998). The visualisationmethod proposed in this paper can improve theinterpretation of the interlandmark data, synthe-sising the information available from the FormDifference Matrix, and allowing a direct com-parison of morphological patterns.

When comparing the airorhynchy in Pongoand Alouatta, some observations can be synthe-sised to consider this interesting parallel evolu-tionary process linking anatomy, ecology, andbehaviour (Fig. 11). In Pongo, Shea (1985) sug-gested that airorhynchy is probably unrelated tomajor local rearrangements, but rather dependson a repositioning of the face compared to theneurocranial structure. Interestingly, this alsoseems to be the case for Alouatta. They share amarked flattening of the orbital/supraorbitalstructures, the orbital shape (tall and narrow),and a consequent mandibular enlargement. Incontrast, the maxillary growth is characterised bya general development and forward projection inthe howlers, and by a sagittal downward stretchin the orangs. In Alouatta and Pongo there is a

63E. Bruner et al.

nuchal flattening, associated with a rotation ofthe occipital foramen. In any case, the braincaseflattening and narrowing in the previous taxon isnot comparable with the braincase verticalstretching and widening of the latter.Furthermore, Pongo does not display the relativecranial base lengthening with the consequentnuchal morphology. The frontal flattening itselfis oriented downward in Alouatta and backwardin Pongo, with respect to to the cranial shape.

In synthesis, in both species airorhynchy ispossibly related to changes in the relationshipbetween face and vault, the consequences ofwhich are mainly found at their structural joint.Actually, the supraorbital structures werehypothesised to represent this architectural inter-face (Lieberman, 2000). Taking into account theanatomical variations of the temporal fossa in theatelids, also the pteric area must be carefully con-sidered. Anyway, the different cranial structure inhowlers and orangs required different rearrange-ments of the whole system.

The complementary role of differentapproaches should be stressed once again.Geometric morphometrics and EDMA are use-ful to consider shape and form respectively.Although the theoretical background of thesemethodologies can be discussed to improve theresolution and power of the morphologicalanalysis (Richtsmeier et al. 2002; Rohlf 2003),they can be used simultaneously to increase therange of available models. Differences betweentheir respective results must not be considerednecessarily as a bias, but in terms of complemen-tary information. In geometric morphometrics,different superimposition procedures can alsocontribute to improve the structural knowledgeof the morphological systems, optimising theshape comparison (General Procrustes Analysis)or considering specific functional networks(Bookstein Superimposition).

All these explorative and descriptive data onthe cranial morphology in Alouatta must be fur-ther developed through the consideration of the

Fig. 11 - Differences between the cranial shape in Alouatta and Pongo. Vectors display thedifferences of the three-dimensional configuration between Alouatta and a con-sensus computed from all the other Atelids (a), and between Pongo and Pan (b)after Procrustes superimposition (solid line: Alouatta and Pongo shapes). Thesuperimposed configurations (c) show a Procrustes comparison between Alouatta(solid line) and Pongo (dashed line).

intra-specific, inter-specific, and inter-genericvariability, especially by analysing the possiblerole of allometry and ontogenetic scaling withrespect to airorhynchy. Some species of howlersshow a sexual dimorphism based on the per-amorphic trajectory in males (Zingeser, 1966),probably related to time-dependent differentialgrowth (Couette, 2002). Furthermore, inAlouatta there are some indications of a possiblefemale size-related selection, and of a relevantmale growth after maturity (Jones et al., 2000).Even more localised differences as the inclinationof the foramen magnum show individual varia-tions (Osman-Hill, 1962). All these data makethe study of structural cranial morphology inAlouatta a quite complex and promising issue.

Acknowledgments

We are grateful to Cristina Giacoma and MarcoGamba, and to all the staff of the 20th Congress ofthe International Primatological Society, in whichthe symposium on geometric morphometrics andprimatology was included. Luca Fiorenza provideduseful anatomical comments. Anna Loy improvedthis paper with constructive comments and advices.

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