Middle phalanx skeletal morphology in the hand: Can it predict flexor tendon size and attachments?

Middle Phalanx Skeletal Morphology in the Hand: Can itPredict Flexor Tendon Size and Attachments?

Mary W. Marzke,1* Marvin M. Shrewsbury,2 and Kristin E. Horner3

1School of Human Evolution and Social Change, Arizona State University, Tempe, AZ 85387–24022Department of Biology, San Jose State University, San Jose, CA 951923Department of Anthropology, Michigan State University, East Lansing, MI 48824

KEY WORDS primate hand; fossil hominins; flexor tendon attachments

ABSTRACT Specific sites on the palmar diaphysis ofthe manual middle phalanges provide attachment forthe flexor digitorum superficialis (FDS) tendon. It hasbeen assumed in the literature that lateral palmar fos-sae on these bones reflect locations for these attach-ments and offer evidence for relative size of the flexortendon. This assumption has led to predictions about rel-ative FDS muscle force potential from sizes of fossae onfossil hominin middle phalanges. Inferences about loco-motor capabilities of fossil hominins in turn have beendrawn from the predicted force potential of the flexormuscle. The study reported here provides a critical firststep in evaluating hypotheses about behavioral implica-tions of middle phalangeal morphology in fossil homi-

nins, by testing the hypothesis that the lateral fossaereflect the size of the FDS tendon and the location of theterminal FDS tendon attachments on the middle pha-lanx. The middle phalangeal region was dissected in 43individuals from 16 primate genera, including humans.Qualitative observations were made of tendon attach-ment locations relative to the lateral fossae. Lengthmeasurements of the fossae were tested as predictors ofFDS tendon cross-sectional area and of FDS attachmenttendon lengths. Our results lead to the conclusion thatthe hypothesis must be rejected, and that future atten-tion should focus on functional implications of the pal-mar median bar associated with the lateral fossae. Am JPhys Anthropol 134:141–151, 2007. VVC 2007 Wiley-Liss, Inc.

One of the anatomical hallmarks of humankind is ourmanual dexterity. As a result, the functional anatomy ofprehistoric hands has received a notable amount ofattention in the literature. Lateral fossae on the palmarradial and ulnar aspects of the middle phalanges ofDigits II–V in fossil hominins have been attributed tothe attachment of the flexor digitorum superficialis(FDS) tendons (Day, 1978; Susman, 1979; Susman andCreel, 1979; Susman and Stern, 1979; Tuttle, 1981; Bushet al., 1982; Ricklan, 1987; Susman, 1988, 1989). The rel-ative size and functional importance of the FDS musclein fossil hominin species have been inferred from quali-tative assessment of the relative size of these lateral fos-sae (Day, 1978; Susman and Creel, 1979; Susman andStern, 1979; Bush, 1982; Stern and Susman, 1983;Ricklan, 1987). For example, Stern and Susman (1983)describe ‘‘concavities for the bifurcate tendon of theFDS’’ (p 282) on the middle phalanges of A. afarensis,which they note exceed the expression in modernhumans, and conclude from these and other features ofthe phalanges that there must have been enhanced ‘‘me-chanical efficiency in power grasping. . .such as occursduring climbing and suspensory behavior’’ (p 284). Sus-man and Creel (1979, p 330) draw the same inference of‘‘strong grasping capabilities’’ and an ‘‘adaptation forclimbing’’ from ‘‘well marked and distally extended inser-tions of m. FDS’’ indicated by topology of the fossil Homohabilis O.H. 7 middle phalanges (p 318). Ricklan (1987,p 661–662), notes for a middle phalanx that ‘‘markeddepressions for the FDS muscle are present, comple-menting the ridges on the sides of the proximal pha-langes, suggesting powerful finger flexors in A. africa-nus.’’ In his view, the phalanges of this species ‘‘showfeatures which would be consistent with fingers well

adapted to powerful gripping actions of the fingers, fromtool using to climbing activities.’’Investigations revealing the lack of relationship

between the size and attachment areas of other muscleshowever have indicated that the nature of such a rela-tionship must be probed specifically and, where possible,quantitatively for the muscles and genera involved(Bryant and Seymour, 1990; Shrewsbury et al., 2003).The purpose of this study is to provide such a probe, bytesting a hypothesis that the location and size of the lat-eral fossae may be explained, in living anthropoid gen-era that possess them, by the location and size of theFDS tendon and its terminal attachments. Two predic-tions of the hypothesis are that:

1. FDS terminal tendons attach exclusively or primarilyinto the lateral fossae.

2. Lateral fossa length is strongly correlated with FDScross-sectional area and terminal FDS tendon attach-ment length.

Grant sponsor: National Institutes of Health, Division of ResearchResources; Grant number: U42 RR15090-01; Grant sponsor: NSF;Grant number: DGE 9987619.

*Correspondence to: Mary W. Marzke, Arizona State University,School of Human Evolution and Social Change, PO Box 872402,Tempe, AZ 85387-2402. E-mail: [email protected]

Received 27 February 2006; accepted 27 March 2007

DOI 10.1002/ajpa.20646Published online 13 June 2007 in Wiley InterScience

(www.interscience.wiley.com).

VVC 2007 WILEY-LISS, INC.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 134:141–151 (2007)

The first prediction is tested with qualitative observa-tions, while the second is tested quantitatively. Theresults are then discussed in relation to interpretation offossil hominin middle phalanges.Testing this hypothesis and others that predict hand

and wrist muscle and joint functions from skeletal fea-tures, is fundamental to tracing the evolution of humancapabilities for effective and habitual tool use and toolmaking, and to discerning locomotor and manipulativecapabilities in hominin ancestors. Skeletal morphologylies at the base of the inferential process from bones offossil species to their functions and ultimately to poten-tial behaviors. If the first step in the inferential process,from bone morphology to functions, is built uponuntested assumptions of bone–muscle relationships, thenthe subsequent inferential process is weak and question-able (Ross et al., 2002). If morphological markers of mus-cle attachments on bone could be identified in the hand,then knowledge about some aspects of finger musclefunctions in living species might be applied to the analy-sis of fossils. For example, it is known that the FDSmuscle is recruited during suspensory behavior of apes(Susman and Stern, 1979). If there were reliablemarkers of FDS attachment size for the tendons on themiddle phalanges, as well as data on the size of the mus-cle and the extent of its recruitment in both locomotorand manipulative behaviors in living apes and humans,then perhaps inferences about FDS muscle size might be

drawn from fossil phalangeal morphology. From theseinferences in turn, the likelihood of suspensory behaviorin the fossil species might be more soundly established.The question of these relationships has been of particu-lar interest with regard to the fossil hominin, Homohabilis, whose middle phalanges share some skeletal fea-tures with living apes (Susman and Stern, 1979; Susmanand Creel, 1979).This study of FDS tendon relationships to middle pha-

langeal skeletal features will, it is hoped, provide a criti-cal first step in evaluating hypotheses about behavioralimplications of middle phalangeal morphology in fossilhominins.The superficial flexor muscle to the ulnar four digits

has a notable evolutionary history. In early reptiles, theFDS tendons originated from muscles intrinsic to thehand. Later, in primitive mammals, the origins of thesemuscles shifted proximally from the hand to the medialepicondyle of the humerus and to a small region runningdiagonally from the proximal anterior medial ulnar shaftdistally onto the radial shaft (Cartmill et al., 1987),thereby recruiting fibers from deeper muscle layers(Lewis, 1989).

Fig. 1. An illustration of the flexor digitorum superficialistendon and its components in a human digit.

TABLE 1. Sample

Genus Common name Age Sex

Homo 1 Human Adult FHomo 2 Human Adult MHomo 3 Human Adult MHomo 4 Human Adult MPan 1 Chimpanzee Infant FPan 2 Chimpanzee Adult MPan 3 Chimpanzee Juvenile MPan 4 Chimpanzee Infant FGorilla Gorilla Infant MHylobates 1 Gibbon Adult FHylobates 2 Gibbon Adult FHylobates 3 Gibbon Infant FHylobates 4 Gibbon Adult FPapio 1 Baboon Infant MPapio 2 Baboon Infant FPapio 3 Baboon Infant MPapio 4 Baboon Adult MPapio 5 Baboon AdultPapio 6 Baboon Adult MPapio 7 Baboon Adult MPapio 8 Baboon Infant MPapio 9 Baboon Infant MPapio 10 Baboon InfantPapio 11 Baboon InfantPapio 12 Baboon InfantMandrillus 1 Mandrill Adult FMandrillus 2 Mandrill Adult MColobus Colobus InfantCercopithecus 1 Guenon Adult MCercopithecus 2 Guenon Adult MAteles 1 Spider monkey AdultAteles 2 Spider monkey Adult FAlouatta Howler monkey Adult FSaimiri 1 Squirrel monkey Adult FSaimiri 2 Squirrel monkey Adult FLeontopithecus Golden lion tamarir Adult FCallithrix 1 Marmoset Adult MCallithrix 2 Marmoset Adult MCallimico Goeldi’s marmoset Adult MGalago Bushbaby Adult FLemur 1 Lemur Adult MLemur 2 Lemur Adult FLemur 3 Lemur Adult F

142 M.W. MARZKE ET AL.

American Journal of Physical Anthropology—DOI 10.1002/ajpa

There is variability among living mammals in the rela-tive size and distribution of FDS muscle origins and inconnections among the muscle bellies (ibid.). The fourinsertion tendons in mammals are positioned in the car-pal canal dorsal to the flexor retinaculum, and pass dis-tally to insert onto the middle phalanges of Digits II–V.Thus the FDS muscle flexes the proximal interphalan-geal joints and also acts on the wrist.In humans, the FDS tendon bifurcates over the proxi-

mal phalanx, exposing the flexor digitorum profundus(FDP) tendon, and forming scisurra bands (Fig. 1) whichpass laterally around both sides of the uncovered FDPtendon to attach as terminal tendons to the radial andulnar margins of the middle phalanx. There is a contra-lateral crossing of some of the medial fibers of the sci-surra bands after they have spiraled around dorsal tothe FDP tendon, referred to as the chiasma tendinum, inwhich some of the medial fibers from the radial scissuraband cross the phalanx to insert with fibers from the ul-nar scissura band on the ulnar margin of the phalanx,and some medial fibers from the ulnar band cross to theradial side, shaping the chiasma tendinum (Shrewsburyand Kuczynski, 1974). Gonzalez et al. (1998) report, how-ever, considerable variability in fiber pattern of thehuman chiasma tendinum.The plate-like chiasma tendinum lies dorsal to the

FDP tendon, forming a sling for it and positioning thedeep tendon to cross the proximal interphalangeal jointat approximately the same position as the FDS tendonbands relative to the flexion/extension axis of rotation(Shrewsbury and Kuczynski, 1974). This positioninghelps to explain a similarity in total excursion by the

superficial and deep tendons reported by Stack (1963),and an increase in FDP excursion when the chiasmatendinum is sectioned longitudinally (Shrewsbury andKuczynski, 1974).Each FDS digital tendon is enclosed, with an accompa-

nying FDP tendon, in a thin sheath filled with synovialfluid that minimizes friction between the two tendonsand contiguous structures. In humans the digitalsheaths are primarily constrained by five annular pul-leys that overlay the synovial sheath, and together withthe underlying phalangeal bones, form fibro-osseouschannels for the synovial sheaths. These five annularpulleys are described and illustrated in the anatomicaland clinical literature as A1–A5 (see Seiler and Lever-sedge, 2000), with A1, A3, and A5 attaching at the pal-mar plates of the metacarpophalangeal, proximal inter-phalangeal, and distal interphalangeal joints, respec-tively, whereas the A2 and A4 pulleys attach to theperiosteal diaphysis of the proximal phalanx and middlephalanx, in that order.The FDS muscle is in a position to flex the proximal

interphalangeal joint independently of the distal inter-phalangeal joint, which is flexed separately by the FDPtendon. When flexion of both joints occurs, FDS actionon the proximal interphalangeal joint comes into play aswhen an increase in gripping force is required (Back-house, 1968; Long, 1968).

MATERIALS AND METHODS

Third and fifth middle phalangeal tendon and skeletalmorphology were compared among 43 individuals from

TABLE 2. Flexor digitorum superficialis tendon and A4 pulley measurements on digit III of adults (mm)a

Specimen

Singletendonwidth

Singletendonheight

Singletendonarea

Rad. tend.attachlength

Uln. tend.attachlength

Rad. tend.distancefrom base

Uln. tend.distancefrom base

Rad. pulleyattachlength

Uln. pulleyattachlength

Homo 1 2.9 2.2 5.0Homo 2 4.8 2.9 10.9Homo 3 5.0 3.9 15.3Homo 4 4.7 3.4 12.5Pan 2 11.8 2.2 20.1 10.2 9.5 8.7 8.5 15.5 15.3Hylobates 1 4.2 1.5 4.9 3.8 3.3 8.6 8.5Hylobates 2 3.6 1.2 3.4 4.7 4.5 7.2 6.9Hylobates 4 2.6 1.1 2.2 4.3 4.8 17.4 17.5 3.8 3.7Papio 4 3.8 2.3 6.9 4.1 4.1 2.4 2.4 5.2 5.2Papio 5 4.1 0.9 2.8 3.9 4.3 3.8 4.6 7.1 6.7Papio 6 5.8 1.0 4.4 7.4 7.2 10.3 10.7 6.3 6.6Papio 7 6.4 0.7 3.4 5.2 6.2 9.8 9.1 2.7 2.6Mandrillus 1 3.4 0.7 1.9 4.2 4.1 9.0 9.2 5.5 6.3Mandrillus 2 2.0 2.0 3.0 1.5 1.2 1.2Cercopithecus 1 3.0 0.6 1.3 2.2 2.2 3.1 3.2 5.7 4.9Cercopithecus 2 2.6 0.7 1.4 1.1 1.4 4.4 4.7 4.2 4.0Ateles 1 3.2 0.6 1.5 2.2 2.4 1.4 1.4 7.5 7.3Ateles 2 2.4 1.1 1.9 3.9 3.5 1.8 1.4 8.2 7.8Alouatta 1.9 0.8 1.2 2.6 2.5 6.0 6.2 7.8 7.2Saimiri 1 1.9 0.4 0.6 0.7 0.7 1.5 1.5Saimiri 2 1.2 0.5 0.5 2.2 2.2Leontopithecus 0.3 0.1 0.0 2.2 2.2Callithrix 1 0.4 0.0 0.0 0.4 0.4 1.8 1.7 1.8 1.7Callithrix 2 0.6 0.1 0.0 0.5 0.4 3.1 3.2Callimico 0.8 0.1 0.1 1.0 0.9 3.9 3.9 1.2Galago 0.2 0.2Lemur 1 0.9 0.5 0.4 1.1 1.0 2.4 2.4Lemur 2 1.9 0.1 0.2 1.8 1.4 3.4 3.5 2.3 2.7Lemur 3 1.4 0.1 0.1 1.0 1.1 3.2 2.8 2.9 2.6

a Missing data: measurements were not obtained.

143MANUAL MIDDLE PHALANX MORPHOLOGY


16 primate genera including humans (Table 1). The sam-ple includes 29 adults and 14 subadults whose epiphyseshave not fused with their respective diaphyses. The thirdand fifth digits were selected so as to span the full rangeof lengths of the middle phalanges. Also, there is vari-ability among humans in occurrence of the FDS tendonto the fifth digit (Baker et al., 1981; Austin et al., 1989;Gonzalez et al., 1997), and it was of interest to see inthis study whether this is also the case in nonhumanprimates. All but two specimens were fresh frozen. Thetwo Cercopithecus hands were preserved in formalin.Data were gathered in two separate phases, first dur-

ing the dissection and second after defleshing the pha-lanx. The hands were dissected with the aid of a light

magnifier and with a dissecting microscope (103) for thesmaller specimens. During the dissection, qualitativeobservations were made for presence/absence of FDStendon bifurcation, chiasma tendinum, and attachmentlocations of FDS terminal tendons relative to the radialand ulnar lateral fossae. These observations were usedfor testing the first prediction of the hypothesis.Also during the dissection, measurements were made

to the nearest 0.1 mm (Tables 2–5), for use in regressionanalyses of skeletal vs. tendon features, which tested thesecond prediction of the hypothesis. The measurementsincluded: radioulnar width and anteroposterior height ofthe FDS tendon proximal to its bifurcation; lengths ofthe radial and ulnar terminal tendon attachments to the

TABLE 4. Flexor digitorum superficialis tendon and A4 pulley measurements on digit V of adults (mm)a

Specimen

Singletendonwidth

Singletendonheight

Singletendonarea







Homo 2 3.8 1.0 3.0Homo 3 2.5 1.6 3.1Homo 4 2.2 1.7 2.9Pan 2 5.2 5.3 7.8 7.1 9.3 9.3Hylobates 1 2.7 0.6 1.2 2.5 3.3 5.3 5.5Hylobates 2 2.1 0.7 1.2 0.2 0.2 6.7 6.7Hylobates 4 0.3 0.3 1.5 1.8Papio 4 4.0 0.5 1.6 5.8 5.0Papio 5 3.5 0.6 1.6 3.7 3.1 5.9 5.5 4.7 5.5Papio 6 4.9 0.7 2.7 3.7 2.8 6.0 7.8 5.1 5.0Papio 7 3.6 0.6 1.8 3.5 2.9 9.0 8.9 4.8 5.0Mandrillus 1 3.5 0.5 1.4 3.1 2.1 10.0 9.4 4.0 3.3Mandrillus 2 2.3 2.8 5.1 4.3 4.3Cercopithecus 1 2.5 0.6 1.1 1.3 1.5 1.9 1.8 2.3 2.8Cercopithecus 2 1.4 0.2 0.2 1.1 1.1 4.5 4.6 2.6 1.9Ateles 1 2.6 0.6 1.1 2.5 2.4 9.2 9.0 5.9 5.4Ateles 2 2.3 1.1 1.9 0.6 3.2 16.5 9.2 3.5 3.8Saimiri 1 1.1 0.1 0.1 1.6 1.6Leontopithecus 0.7 1.5 1.5Callithrix 1 0.4 0.0 0.0 0.1 0.3 1.5 1.4 1.1 0.9Callithrix 2 0.2 0.1 0.0 0.3 0.3 1.8 1.9 1.6 1.8Callimico 0.6 0.5 2.6 2.6Galago 0.3 0.3 0.1 2.6 2.4Lemur 1 1.8 0.1 0.1 2.3 2.1Lemur 2 1.1 0.1 0.1 1.2 1.3 4.6 4.5 3.4 3.5Lemur 3 0.9 0.1 0.1 1.8 1.8 2.0 2.5


TABLE 3. FDS tendon and A4 pulley measurements on digit III of subadults (mm)a

Specimen

Singletendonwidth

Singletendonheight

Singletendonarea







Pan 1 5.1 0.7 2.7 3.6 3.5 10.0 10.4 6.2 6.1Pan 3 2.1 0.8 1.3 1.8 1.4 4.0 4.0 5.2 5.1Pan 4 3.3 0.8 2.2 2.0 1.9 3.7 3.5 3.4 4.1Gorilla 4.7 0.7 2.5 3.9 3.2 5.3 5.4Hylobates 3 1.1 0.2 0.2 0.9 0.8 2.2 2.4 2.1 2.4Papio 1 3.8 0.4 1.2 2.1 1.4 1.4 1.5Papio 2 2.2 0.3 0.5 1.4 1.6 3.1 3.1Papio 3 2.8 1.4 3.1 2.3 2.2 2.9 2.9Papio 8 2.3 0.3 0.6 2.4 2.4 4.1 4.1Papio 9 2.5 0.4 0.8 1.2 1.3 1.5 1.5Papio 10 1.8 0.3 0.4 1.3 1.3 1.3 1.3Papio 11 1.6 0.3 0.4 0.5 0.5Papio 12 2.2 0.4 0.7 1.5 1.5Colobus 1.4 0.1 0.1 1.2 1.2




middle phalanx, measured from the most proximal tothe most distal fibers; and distance from the phalangealbase (on the side of the FDS attachment) to the proximalend of the tendon attachment.The cross-sectional area of the FDS tendon was calcu-

lated using the formula for area of an ellipse. Previouswork by An et al. (1981) has shown that tendon cross-sectional areas have a direct relationship to potentialtendon forces, and that there is a close correlationbetween tendon cross-sectional area and its associatedmuscle physiological cross-sectional area, which is pro-portional to muscle force potential. It is thereforeassumed here that any skeletal features found to bestrongly correlated with FDS tendon cross-sectional areawould be excellent predictors of both flexor tendon sizeand associated muscle force potential.Following defleshing and cleaning of the bones, the

palmar surface of the middle phalanges was examinedclosely for patterns of occurrence and relationshipsamong skeletal features, including the palmar medianbar, lateral fossae, and lateral ridges (Fig. 2). Theseobservations contributed to further qualitative testing ofthe first prediction of the hypothesis. Measurementswere made of lateral fossa length where fossae werepresent (Fig. 2; Tables 6 and 7), for use in the regressionanalyses testing the second prediction of the hypothesis.The length of each lateral fossa was measured from theproximal to the distal end of the concavity. Fossa shapeis generally oval, but with small attenuations that affectthe precise determination of measurement points. Dis-tance to the fossa was measured from the proximal endsof the fossa to the base of the phalanx on the same side(Fig. 2). Measurements of these variables repeated on aspecimen in three different sessions indicate a meanerror of 0.08. Measurements were also made of middlephalanx length, width of the base, and width at midshaft(Fig. 3; Tables 6 and 7). A geometric mean of these threevariables was calculated for use as an estimator of bodysize (Jungers et al., 1995) in standardizing the fossalength and tendon size variables for the regressionanalyses.The genera were then compared qualitatively in their

patterns of relationships of tendon and skeletal featuresto test the first prediction of our hypothesis. For thequantitative test of the second prediction of the hypothe-sis, least squares regression analysis was applied to

standardized fossa length, tendon cross-sectional area,and terminal tendon length measurements to discernskeletal predictors of FDS tendon size in our primatesample. Analyses were not run for samples that had

TABLE 5. Flexor digitorum superficialis tendon and A4 pulley measurements on digit V of subadults (mm)a

Specimen

Singletendonwidth

Singletendonheight

Singletendonarea







Pan 1 3.6 0.3 0.7 1.8 1.8 7.1 8.0 4.5 4.2Pan 3 0.7 0.3 0.1 0.2 0.8 2.1 2.1 2.2 1.9Pan 4 1.3 0.5 0.5 0.9 0.9 2.3 2.6 1.7 1.7Hylobates 3 2.2 0.9 1.6 3.2 2.3 8.5 6.8Papio 1 1.4 0.1 0.1 1.4 1.4Papio 2 1.7 0.1 0.1 2.8 2.8Papio 3 1.4 0.4 0.4 1.7 1.7Papio 8 1.3 0.3 0.3 1.8 1.8 2.6 2.4Papio 9 1.0 0.1 0.1 1.4 1.4Papio 10 0.5 0.5 0.2 1.9 1.9Papio 11 1.3 0.3 0.3 1.2 1.2Papio 12 1.7 0.1 0.1 2.5Colobus 0.4 0.1 0.0 1.6 1.6


Fig. 2. Illustration of a manual middle phalanx of Digit IIIfrom a gibbon showing features observed. Brackets mark theproximal and distal limits of the fossa length measurement andthe proximal and distal limits of projection of the lateral ridgein this specimen.



fewer than eight individuals with data for the relevantpairs of variables. Significance of an association betweenx and y was set at P < 0.05.Following these comparative observations and quanti-

tative analyses of relevant features of middle phalanxtendo-skeletal anatomy in the living genera, observa-tions were made on casts of fossil hominin middle pha-langeal skeletal morphology. These included a cast of theAL 333 w-46 middle phalanx of Australopithecus afaren-sis, provided by the Institute of Human Origins, ArizonaState University, and a cast of the immature Homohabilis longest middle phalanx (lacking an epiphysis),from the Kenya National Museum.

RESULTS

Observations of the palmar median bar, medianfossa, lateral fossae, and ridges

General comparative observations of middle phalan-geal bone morphology show a considerable amount ofvariability among genera and among individuals withingenera, in the presence and associations of features onthe palmar surface of the middle phalanx in both thethird and fifth digit. Several specimens have a rounded

relief of bone forming a palmar median bar running lon-gitudinally along the shaft (Fig. 2). The bar occupiesvarying portions of the palmar surface along its midlineand may broaden at the proximal and/or distal ends ofthe shaft to become continuous with a surface that ispalmarly elevated from one side to the other. Betweenthe bar and the radial and ulnar margins of the shaft,palmar lateral fossae (Fig. 2) are generally found. Theseappear to be simply the regions of the shaft that are notpalmarly elevated in the midline. Their locations corre-spond to the location of the bar; wherever the lateral fos-sae occur, the palmar median bar (previously referred toas a ‘‘keel’’ by Walker and Leakey (1993) and by Begun(1988, 1993), and Begun et al. (1994)) is also present. Insome individuals the palmar median bar covers almostthe entire length of the shaft, whereas in others it is re-stricted to the middle of the shaft or to the proximal ordistal end of the bone’s diaphysis.In other specimens lacking a palmar median bar with

accompanying lateral fossae, the entire palmar surfaceof the shaft is flat, or in some specimens it appears hol-low, forming a palmar median fossa if ridges along thelateral margins project markedly anteriorly. Such ridgesproject from the lateral palmar margins of the middlephalanx in many genera and over varying lengths.

TABLE 6. Measurements of the third middle phalanx (mm)a

SpecimenRad. fossalength

Uln. fossalength

MPb

lengthMP basewidth

MP mid-shaftwidth

Geometricmeanc

AdultsHylobates 1 8.5 6.0 28.7 6.9 4.8 9.8Hylobates 2 9.1 8.2 29.3 5.3 4.3 8.7Hylobates 4 13.0 11.4 35.0 7.6 7.2 12.4Mandrillus 1 9.4 9.0 21.4 7.9 5.8 10.0Cercopithecus 1 5.2 4.7 12.8 4.6 3.2 5.7Cercopithecus 2 2.7 4.1 11.7 4.1 2.7 5.1Ateles 1 8.1 8.9 26.5 7.2 5.4 10.1Ateles 2 6.3 28.6 7.9 5.3 10.6Alouatta 3.2 3.8 21.5 6.6 5.1 8.9

SubadultsPan 1 5.3 5.8 16.3 6.7 6.5 8.9Pan 3 4.8 4.9 15.5 5.7 5.9 8.1Hylobates 3 3.3 3.4 12.2 3.7 3.8 5.5

a Missing data: features were not present.b MP: middle phalanx.c Geometric mean: cube root of product of middle phalanx length, base width and midshaft width.

TABLE 7. Measurements of the fifth middle phalanx (mm)a

SpecimenRad. fossalength

Uln. Fossalength

MPlength

MP basewidth

MP mid-shaftwidth

Geometricmeanb

AdultsPan 2 5.4 4.8 30.0 11.8 8.0 14.1Hylobates 1 3.2 3.1 18.8 3.7 3.4 6.2Hylobates 2 3.2 2.3 19.1 5.1 3.7 7.1Mandrillus 1 7.1 6.7 16.4 6.6 4.4 7.8Cercopithecus 1 2.5 2.4 8.9 3.7 2.4 4.3Cercopithecus 2 2.7 2.5 8.8 3.3 2.3 4.1Ateles 1 6.4 8.2 23 6.1 4.1 8.3Callithrix 1 1.6 1.3 6 2.5 1.2 2.6Callithrix 2 1.1 1.0 5.9 2.4 1.1 2.5

SubadultsPan 1 3.9 4.4 10.4 4.6 4.7 6.1Pan 3 2.5 2.9 8.7 3.3 3.5 4.7Hylobates 3 2.9 2.6 8.4 2.6 2.6 3.9

a Missing data: features were not present.b Geometric mean: cube root of product of middle phalanx length, base width and midshaft width.



In some specimens, one portion of the ridge projects fur-ther in a palmar direction than the rest, suggesting afocus of strain on the A4 annular pulley fibers by thedeep flexor tendon during distal interphalangeal flexion.There is not a constant association of lateral ridges withthe palmar median bar and lateral fossae.The features of the middle phalangeal palmar surface

described above are distributed as five different patternsin the sample for the third digit, as follows: (1) 12 of the42 individuals for whom data on skeletal topology of theDigit III middle phalanx are available have a palmarmedian bar flanked on either side by lateral palmar fos-sae, along with ridges on the phalangeal lateral margins.These include two subadult chimpanzees, three adultand one subadult gibbon, one adult mandrill, two adultguenons, two adult spider monkeys (one with only a ra-dial fossa), and the adult howler monkey. (2) A palmarmedian bar and ridges, without palmar lateral fossae,occur in the Digit III middle phalanx of one human and

two squirrel monkeys. (3) There are lateral ridges withneither a palmar median bar nor lateral fossae in theDigit III middle phalanx of one human, two subadultbaboons, one marmoset and the Goeldi marmoset. (4)The palmar median bar, palmar lateral fossae and ridgesare all absent in six subadult baboons, the subadult colo-bus monkey, the golden lion tamarin, the galago and onelemur. (5) A wide palmar median fossa flanked by ridgesis present in two humans, the adult chimpanzee, fouradult baboons, one marmoset, and two lemurs. The pal-mar median fossa tends to be triangular in the baboons,bordered by thick, rough ridges.

Observations of FDS tendon attachmentsrelative to skeletal features

There is considerable variability among genera, andamong individuals within genera, in the locations of theattachments of the terminal FDS tendons relative to thelateral fossae. In all genera, the tendon bifurcates overthe proximal phalanx and sends ulnar and radial scis-sura bands around the lateral sides of the FDP tendonto a position dorsal to the deep flexor’s surface. Achiasma tendinum was present in the third finger of 36of 37 specimens and in the fifth finger of 35 of 39 speci-mens in which its presence or absence was noted. It wasmissing in the subadult gorilla third and fifth fingersand in the fifth finger of the adult chimpanzee, a suba-dult baboon and the galago.The FDS terminal bands attached near the lateral

margins of the third and fifth middle phalanges, withthe insertions beginning at varying distances from themiddle phalangeal base. The attachment was neverexclusively into the lateral fossae, where fossae werepresent, but occasionally fibers inserted into part of thefossa as well as variably more proximally or distally. Thefossae were actually filled by fat pads in a mandrill andin a gibbon, and the tendons attached elsewhere. Inmany of the phalanges of our sample there were no lat-eral fossae, yet the FDS tendons reached the middlephalanx of all but the fifth digit of one human. In sev-eral specimens the FDS attachments were into part ofthe lateral ridges or into part of the base of the ridges,proximal to the ridges on the margin of the bone, or intopart of the inner surface of the A4 annular pulley, whichattaches to the lateral margins of the phalanx shaft. Inall four humans there was periosteal bone proliferationalong the inner sides of the lateral ridges of the thirdmiddle phalanges, at locations where parts of the FDStendon attached. Similar bone proliferation is seen inboth guenon specimens and in one mandrill.Following is a description of FDS tendon attachments

relative to the lateral fossa on the radial side of the thirdmiddle phalanx in two adult specimens (Fig. 4) and intwo subadult specimens, illustrating some of the dramaticdifferences between genera found in our dissections. Lat-eral ridges are shown in the figure, with brackets indicat-ing their approximate proximal and distal limits.

1. Ateles 2 (adult, Fig. 4A): The FDS tendon attachmentlies entirely proximal to the lateral fossa, beginningonly 1.8 mm from the base of the middle phalanx andrunning distally 3.9 mm along the radial margin (thelateral fossa is 6.3 mm long, beginning 7.0 mm fromthe base).

2. Hylobates 4 (adult, Fig. 4B): The FDS tendon attach-ment begins 17.4 mm from the base of the phalanx

Fig. 3. Illustration of a manual middle phalanx of a gibbon,showing measurements made for calculation of the geometricmean used as an estimator of body size.



and runs distally in the lateral fossa along the innermargin of the lateral ridge over a distance of 4.3 mm(the lateral fossa is 13 mm long and begins 9.7 mmfrom the base).

3. Hylobates 3 (subadult): The FDS tendon attachmentbegins 2.2 mm from the epiphyseal surface at thebase of the shaft and extends distally 0.9 mm, lyingwithin the lateral fossa along the inner side of the lat-eral ridge (the lateral fossa, 3.3 mm long, begins 2.6mm from the epiphyseal surface).

4. Pan 1 (subadult): The FDS tendon attachment liesentirely distal to the lateral fossa, beginning 10 mmfrom the epiphyseal surface at the base of the shaftand inserting into the ridge over a length of 3.6 mmdistally (the lateral fossa begins 3.6 mm from the epi-physeal surface and runs distally 5.3 mm).

Ateles 1 and Hylobates 1 and 2 recall the above adultAteles and Hylobates specimens in their FDS attachmentsrelative to the fossae. However, the FDS attachment in

Hylobates 4 begins proportionately further from the baseof the phalanx than in the other two adult Hylobates. Inadults of other genera with a radial fossa, the tendoninserts into the proximal half of the fossa in Cercopithe-cus 1 and 2, into the distal half of the fossa in Mandrillus1, and into the distal part of the fossa and along the lat-eral ridge of the phalanx beyond the fossa in Alouatta.In genera without lateral fossae, FDS tendon attach-

ment lengths were quite similar among individualswithin genera. However, there was variability among thefour adult baboons in the relative distance to the mostproximal FDS attachment fibers.It is noteworthy that the FDP tendon attached just

proximal to the head of the middle phalanx and volarplate as well as to the base of the distal phalanx in eightsubadult and adult baboons in which the FDP was fol-lowed to its insertions). This middle phalangeal insertionwas not seen in gibbons, squirrel monkeys, the colobusmonkey, the golden lion tamarin, galago, or lemur inwhich the FDP insertions were examined in detail.

Fig. 4. Illustration of manual middle phalanx of Ateles 2 (A) and Hylobates 4 (B) showing the location of the radial FDS tendonattachment relative to the radial lateral fossa and the lateral ridge.



The FDS tendon to the fifth digit was very thin inspecimens from several genera (two infant baboons, theinfant colobus monkey, an adult squirrel monkey and anadult lemur). It was absent altogether in one humanspecimen (Homo 1). In another human the tendon didnot bifurcate and had a single insertion into the radialside of the phalanx. The tendon attached to the base ofthe phalanx in the fifth middle digits of an infant baboonand a lemur. Tendon attachments relative to skeletalfeatures were similar to those of the third digit in somebut not all individuals.

Quantitative analysis: Skeletal predictors of FDStendon size and attachment lengths

The regression analyses testing the second predictionof the hypothesis show that lateral fossa lengths on thethird and fifth middle phalanges do not reliably predicteither the FDS tendon cross-sectional area or the FDSterminal tendon attachment lengths. No significant cor-relations were found between the standardized skeletaland tendon variables (Table 8).

DISCUSSION AND CONCLUSIONS

What can we learn from lateral fossa locationsand sizes?

To review, the hypothesis addressed in this study pre-dicts that the locations and lengths of the palmar lateralfossae on the middle phalanx are useful indicators ofFDS terminal tendon location and size in primates. Thehypothesis was tested by comparative qualitative obser-vations of all attachment locations for FDS tendon fibersrelative to the lateral fossae and by regression analysisof fossa lengths vs. tendon measurements. The hypothe-sis is rejected for the following reasons. First, the com-parative observations from dissections show that theFDS tendon did not in any case insert exclusively intothe lateral fossae or occupy the full fossae in either thethird or the fifth middle phalanx. The FDS terminal ten-dons insert into the palmar aspect of the middle phalan-geal shaft near the lateral margins, at varying distancesfrom the base, with fibers running variably to parts ofthe fossae, the palmar region proximal to and/or distal tothe fossae, and the region of the lateral ridges and adja-cent annular pulley attachment fibers.Second, where there are lateral fossae, results of the

regression analyses show that the fossa lengths (whenthey are standardized for body size by the geomean) donot reliably predict standardized FDS tendon cross-sectional area or terminal radial and ulnar tendon attach-ment lengths. This finding is not surprising, in view of thequalitative observations showing a lack of consistent mu-tual distribution of the skeletal and tendon features.If the development of lateral fossae cannot be ex-

plained by FDS attachments and by stresses associatedwith FDS muscle activity, why do they occur on the mid-

dle phalanges? One possible explanation may be foundin the fact that when they do occur, they are invariablyaccompanied by a palmar median bar. The fossae there-fore may be simply the regions of the palmar surfacethat are not thickened anteriorly into a bar. Perhapsthis palmar bar develops in response to loading, asBegun et al. (1994) have suggested for median bars(which they call ‘‘median keels’’) in the pedal middlephalanges of Proconsul. They suggest that this midlinethickening of the bone probably reflects (along withdorso-ventral robusticity of the bone) dorso-ventrallydirected bending stress that accompanies the pull ofpowerful digital flexors and substrate reaction force. Asystematic comparative biomechanical analysis of thesize and shape of the bar and loading of the middle pha-langes of the hands and feet associated with locomotorand manipulative behaviors would be required to testthis hypothesis. On the other hand, the palmar medianbar may be, as Walker and Leakey (1993) indicate, sim-ply a byproduct of the bilateral fossa excavations. In thiscase an explanation other than FDS attachments mustbe found to explain why hollowing of the phalanx wouldoccur along the radial and ulnar margins of the boneover varying extents in some genera.

Differences between third and fifth digit FDS

It was found that the FDS tendon to the fifth fingerwas absent in one of the four humans and lacked an ul-nar insertion in a second human, whereas it was presentin all the third middle phalanges. The tendon was pres-ent but relatively small in many of the nonhuman pri-mates. Patterns of tendon attachments were not consis-tently the same as those of the third middle phalanx.Our finding for humans recalls that of Shrewsbury

and Kuczynski (1974), who report the absence of theFDS tendon and chiasma tendinum in Digit V for four oftwenty human cadavers in their sample. However, theyfound in these individuals radial and uncrossed bands aswell as scissura bands, which emerged from surroundingsynovial tissue or from the underside of the proximalflexor sheath. Two additional cadavers had only a radialcrossed band. Where it was present, the FDS tendonwas observed to be less developed than in the more ra-dial digits (ibid.). Results of other studies (Baker et al.,1981; Austin et al., 1989; Gonzalez et al., 1997) agreewith previously published work on human cadavericmaterial.

Comparative middle phalanxskeletal morphology

Variability between and within genera in patterns oftopologic features of the middle phalanx indicates thatthere must be a complex interrelationship of genetic andepigenetic factors involved in tendo-skeletal developmentof this region. For example, all the adult and subadultgibbon third middle phalanges exhibit a palmar median

TABLE 8. Regression analyses

Analysis

Digit III Digit V

R2 N P-value R2 N P-value

Rad. fossa length vs. FDS tendon area 0.12 9 0.36 0.01 8 0.80Uln. fossa length vs. FDS tendon area 0.00 8 0.94 0.05 8 0.60Rad.fossa length vs. rad. tendon length 0.38 9 0.08 0.05 9 0.56Uln. fossa length vs. uln.tendon length 0.21 8 0.25 0.01 9 0.82



bar and lateral fossae, in contrast to all adult and suba-dult baboons, which lack a palmar median bar and lat-eral fossae. Within gibbons, adults and subadults sharenot only the bar and lateral fossae but also lateralridges. Yet within Papio, the adult specimens have me-dian fossae bordered by ridges, whereas the middle pha-langeal shafts of the subadults are relatively featureless,with the exception of small lateral ridges in two of thesubadults. Within Pan, a palmar median bar with lateralfossae and ridges was found in two subadult individuals,but the adult had a median fossa with marginal ridges.Thus, there tend to be differences between adults andsubadults in the skeletal topology we have observed insome genera, but not in all. It would be interesting toinvestigate the kinematics and biomechanics of the mid-dle phalanges associated with locomotor and manipula-tive behaviors, and to identify morphological correlatesof functional differences not just between genera butalso between subadults and adults within genera.

Middle phalanx morphology in fossil hominins

It is concluded from the comparative qualitative obser-vations and quantitative analysis of middle phalanxmorphology in the living primate sample that the sizeand location of its lateral fossae cannot serve as reliablepredictors of FDS size or location in fossil hominins.How, then, can one explain the presence and relative

size of lateral fossae in adult middle phalanges of all fos-sil hominin genera whose middle phalanges have beenrecovered? Possibly an explanation may be found in theconsistent pattern of association of the fossae with a pal-mar median bar. For example, the longest (presumablythird) middle phalanges of A. afarensis, and Homohabilis hands have a palmar median bar flanked by lat-eral fossae. This pattern is illustrated well in (Napier,1962, Fig. 1) and is described and illustrated by Susmanand Creel (1979, Fig. 8) and Bush (1982, Fig. 9). TheParanthropus middle phalanges from Member I, Swartk-rans are described by Susman (1989) as having pro-nounced markings for insertion of the FDS. A palmarmedian bar with lateral fossae may be seen in Figure10.6 of this paper. According to Walker and Leakey(1993), the palmar surface of the Homo ergaster middlephalanx has a very strong ‘‘bilateral excavations extend-ing for about half the length of the shaft,’’ and the exca-vation leaves what they call a proximal midline ‘‘keel’’over the proximal half. Lorenzo et al. (1999) reportmarked insertion areas for the FDS on the diaphysis ofmiddle phalanges of Homo antecessor. In their Figure 1k, a palmar median bar may be seen along the palmarsurface of a middle phalanx shaft, separating radial andulnar lateral fossae. The results of the present studysuggest that attention should be focused on the palmarbar as well as on the lateral fossae, in future attempts topredict internal and external stresses on the bone inliving and fossil primates.

ACKNOWLEDGMENTS

We thank the following for dissection specimens: thePrimate Foundation of Arizona, L. Bodell, M.D., South-western Research Station, the Phoenix Zoo, WildlifeWorld Zoo, Sacramento Zoo, and the Camaron Park Zoo.E. Landis and B. Szymik helped with dissections and T.Kivell kindly provided data on the gorilla. We are grate-

ful to D. Hawkey for technical assistance and D. Youngfor helpful discussions concerning data analyses. We alsothank S. Selkirk for Figures 2 and 4. R. Marzke’s contri-butions at all stages were invaluable. The chimpanzeecadaver data collection was approved by the PrimateFoundation of Arizona Institutional Animal Care andUse Committee and was supported, in part, by theNational Institutes of Health Division of ResearchResources, Grant U42 RR15090-01.

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Middle phalanx skeletal morphology in the hand: Can it predict flexor tendon size and attachments?