Primate postcrania from the late middle Eocene of Myanmar

Abstract

Fossil primates have been known from the late middle to late Eocene Pondaung Formation of Myanmar since the description of Pondaungia cotteri in 1927. Three additional primate taxa, Amphipithecus mogaungensis, Bahinia pondaungensis and Myanmarpithecus yarshensis, were subsequently described. These primates are represented mostly by fragmentary dental and cranial remains. Here we describe the first primate postcrania from Myanmar, including a complete left humerus, a fragmentary right humerus, parts of left and right ulnae, and the distal half of a left calcaneum, all representing one individual. We assign this specimen to a large species of Pondaungia based on body size and the known geographic distribution and diversity of Myanmar primates. Body weight estimates of Pondaungia range from 4,000 to 9,000 g, based on humeral length, humeral midshaft diameter, and tooth area by using extant primate regressions. The humerus and ulna indicate that Pondaungia was capable of a wide variety of forelimb movements, with great mobility at the shoulder joint. Morphology of the distal calcaneus indicates that the hind feet were mobile at the transverse tarsal joint. Postcrania of Pondaungia present a mosaic of features, some shared in common with notharctine and adapine adapiforms, some shared with extant lorises and cebids, some shared with fossil anthropoids, and some unique. Overall, Pondaungia humeral and calcaneal morphology is most consistent with that of other known adapiforms. It does not support the inclusion of Pondaungia in Anthropoidea.

The first fossil primate described from Myanmar was Pondaungia cotteri Pilgrim in 1927 (1) from a locality near Pangan (Pankan) village in the Pondaung Formation of central Myanmar (formerly Burma). Ten years later Colbert (2) described Amphipithecus mogaungensis from near Mogaung village in the Pondaung Formation. No other primates were reported from the Pondaung Formation over the next 42 years until four new specimens were discovered at Mogaung in 1978 (3–5). Several new specimens of primates have been reported subsequently from the two earlier areas along with specimens from new localities near Bahin, in the Pondaung Formation (5–9). Mogaung localities are middle Eocene (late Lutetian to early Bartonian) while localities near Pangan and Bahin are late middle (late Bartonian) to late (Priabonian) Eocene (10). A Bartonian age for localities in the Bahin area is supported by a fission-track date of 37.2 ± 1.3 mega-annum (Ma) on zircon crystals from a tuffaceous bed that outcrops at several localities (35).

Primates known from Myanmar include at least four taxa, the original two species plus Bahinia pondaungensis (7) and Myanmarpithecus yarshensis (36). An additional species of Pondaungia, P. minuta [holotype NMMP (National Museum of Myanmar Primate) 4] was proposed by Jaeger et al. (6), and another species of Amphipithecus, “A. bahinensis” (NMMP 7) was informally cited by Thein (8). Jaeger et al. (6) questioned the distinctiveness of A. bahinensis, instead regarding it as A. mogaungensis, while Takai et al. (5) have questioned the validity of P. minuta, a species based on a heavily worn and eroded specimen.

New discoveries of primate remains from the Pondaung Formation are the result of a Myanmar joint government-university initiative begun in 1997 by the Office of Strategic Studies, Ministry of Defense and the University of Taunggyi, Dagon University, and Hlaing College. In April 1997 this team discovered new fossil localities in the Bahin area (Fig. 1) that led to the recovery of the first complete jaw of Amphipithecus mogaungensis now designated NMMP 7. At this point, an invitation was made to one of us (R.L.C.) to mount a joint Myanmar-American field project to the Bahin area. On December 26, 1997 members of this international team discovered the first primate postcrania in the Pondaung Formation at a locality less than 2 km from Yarshe kyitchang where NMMP 7 was found (Fig. 1).

Figure 1.

(A) Map of Myanmar shows the location of Bahin fossil sites about 300 km southwest of Mandalay. (B) Bahin area map depicts localities yielding Amphipithecus jaw, NMMP 7, (Yarshe, 21° 44′ 13"N, 94° 38′ 12"E) and Pondaungia humeri, ulnae and calcaneum, NMMP 20, (Pk1, 21° 45′ 13"N, 94° 38′ 33"E). These Global Positioning System (GPS) coordinates mark the precise location of each specimen. The Yarshe and Pk1 localities, depicted as patterned ovals in B, represent the areal extent of the outcrops used to produce the measured stratigraphic sections presented in C and D. Age of Amphipithecus in C is based on micropaleontological samples and inferred nannozone assignment as well as vertebrate faunal associations. Age of Pondaungia postcrania in D is inferred by faunal comparisons with other localities in the Bahin area. No micropaleontological samples suitable for analysis have been found in D. However, a tuffaceous layer recently found in this section has been dated by fission-track (35) and confirms a Bartonian age for the Pondaungia postcrania. Nearby locality Pk2 in B has recently yielded a new dentary of Pondaungia sp nov. (37).

Pondaungia Postcrania

All known primate specimens from the Pondaung Formation are dental and cranial remains. Field collecting at a locality about 4 km NW of the village of Bahin (Fig. 1) resulted in the discovery of some associated postcranial elements (NMMP 20) of a relatively large-bodied primate (11). These remains had eroded from a dark red-brown mudstone on a small hillock undistorted by local dipping. The local name for this locality is Sabapondaung kyitchang; it also has been cataloged as Pk1 (see figure 5 in ref. 12). We have assigned these postcrania to Pondaungia as it is the largest of the four primate genera now known from the Bahin area (Fig. 2). Pondaungia is also the most common primate in the Pondaung Formation, representing 50% of the 20 primate specimens recovered to date.

Figure 2.

Distribution of estimated body weights of Myanmar primates compared with two notharctines, one lemuriform and one platyrrhine. Body weight estimates of fossil taxa are based on tooth size for all taxa except Pondaungia postcrania, which is based on humeral length and humeral midshaft diameter (13, 14).

NMMP 20 includes a nearly complete left humerus, missing only fragments of the supinator crest, a right humerus with a complete proximal end, a portion of the shaft, and a broken distal end, a right proximal ulna preserving the distal part of the trochlea and the radial articular surface, a left proximal ulna preserving the olecranon process and proximal trochlea, the distal half of a left calcaneum, two other long bone shaft fragments, and a fragmentary vertebral centrum (Figs. 3–5).

Figure 3.

Right humerus (reversed) of Smilodectes mcgrewi [University of Michigan (UM) 100603] in posterior (A) and anterior (B) views; left humerus of Pondaungia (NMMP 20a) in posterior and proximal (C), medial (D), and anterior (E) views, portion of right humerus (NMMP 20b) in anterior view shown in E to indicate extent of supinator crest; left humerus of Aegyptopithecus zeuxis (Duke Primate Center 1275) in posterior (F) and anterior (G) views. Circled numbers denote the following features of Pondaungia: 1) rounded, proximally extended head; 2) very reduced deltopectoral crest; 3) extensive supinator crest; 4) presence of entepicondylar foramen (arrows on all figures indicate foramen); 5) rounded capitulum separated from trochlea by gutter; 6) absence of dorsoepitrochlear pit [note presence of deep pit in Aegyptopithecus (F)]. Line in D indicates proximoposterior orientation of humeral head in Pondaungia. Scales represent 1 cm.

Figure 5.

Calcaneocuboid facet of (A) Pondaungia (NMMP 20e), (B) Nycticebus coucang (University of Michigan Museum of Zoology, UMMZ 113354), (C) notharctine adapiform Cantius (UM 80737), (D) adapine adapiform A. parisiensis (unnumbered cast in UM collection), (E) omomyid Omomys (UM 98604), and (F) Saguinus sp. (unnumbered specimen in UM collection). All specimens are drawn to the same size. Scales represent 1 cm.

The humerus of Pondaungia (Fig. 3 C–E) is 95.6 mm in length (see Tables 1 and 2 for humeral and calcaneal measurements), comparable to humeral length in extant ring-tail lemurs (Lemur catta). Based on humeral length/midshaft diameter to body weight relationships (13, 14), we estimate the body weight of Pondaungia to have been between 5 and 6 kg. This compares favorably with an estimated body weight of 4 to 9 kg for all specimens of Pondaungia by using tooth size as a proxy for body weight (15).

Table 1.

Distal humeral indices after Szalay and Dagosto (22)

Locomotor category	Taxon	TAI	THWI	TCI	RTWI	MEI	AI
Arboreal quadruped	Varecia variegata	44.5	86.9	88.2	80.4	18.7	82.1
	Lemur catta	47.8	101.6	103.4	81.3	12.8	79.1
	Cheirogaleus major	43.9	80.3	85.6	79.2	22.3	71.1
	Hapalemur griseus	41.0	81.3	66.7	70.8	25.4	70.0
	Mean	44.3	87.5	86.0	77.9	19.8	75.6
Vertical clinging and leaping	Indri indri	34.7	111.8	64.2	53.0	12.5	80.9
	Propithecus verreauxi	31.1	136.3	46.6	45.0	19.5	74.4
	Avahi laniger	36.5	112.8	51.4	57.4	21.6	72.1
	Galago senegalensis	43.0	107.1	75.9	72.4	28.8	71.1
	Tarsius sp.	40.0	130.6	66.5	66.7	25.7	60.8
	Mean	37.1	119.7	60.9	58.9	21.6	71.9
Slow climbing	Perodicticus potto	33.6	124.3	45.7	50.7	29.3	72.6
	Nycticebus coucang	38.5	131.3	57.8	62.5	23.6	74.3
	Loris tardigradus	32.8	170.5	43.7	48.9	16.6	76.6
	Mean	35.0	142.0	49.0	54.0	23.2	74.5
Fossil taxa	Pondaungia	47.3	95.0	110.1	89.9	25.0	62.4
	Smilodectes gracilis	35.5	106.1	55.8	55.1	27.5	68.5
	Adapis parisiensis	39.9	75.9	65.5	66.1	22.6	69.5
	Shoshonius cooperi	48.8	76.2	—	150.0	—	70.5
	Omomys carteri	40.9	100.0	—	69.2	—	68.8
	Aegyptopithecus zeuxis	47.9	82.9	108.9	92.1	27.1	70.6

TAI, trochlear articular index; RTWI, relative trochlear width index; THWI, trochlear height-width index; MEI, medial epicondylar index; TCI, trochlear-capitular index; AI, articular index. 

Table 2.

Calcaneal measurements and indices after Gebo et al. (29)

Taxon	C2	C3	C4	C5	C6	C8	C4/C3	C6/C5
Calcaneal measurements
Pondaungia	13.3	9.5	5.1	6.8	9.2	11.9
Cantius ralstoni	6.6	5.6	2.2	4.6	3.3	7.4
Cantius mckennai	7.8	5.5	2.9	5.2	4.0	8.2
Cantius trigonodus	8.9	6.9	3.2	4.9	3.7	8.8
Cantius abditus	10.2	7.6	3.7	6.5	4.8	9.6
Notharctus venticolis	12.0	8.7	4.1	7.8	6.0	10.4
Notharctus tenebrosus	11.6	7.1	4.1	7.6	6.3	9.1
Smilodectes gracilis	10.7	8.0	3.9	5.5	4.7	10.5
A. parisiensis	7.1	5.5	3.5	5.0	5.0	4.9
A. magnus	12.4	10.6	5.9	9.5	8.9	10.8
Omomys carteri	5.1	3.1	2.2	3.5	2.5	7.6
Calcaneal indices
Pondaungia							53.7	135.3
C. ralstoni							39.3	71.7
C. mckennai							52.7	76.9
C. trigonodus							46.3	75.5
C. abditus							48.7	73.8
N. venticolis							47.1	76.9
N. tenebrosus							57.7	82.9
S. gracilis							48.8	85.5
A. parisiensis							63.6	100.0
A. magnus							55.7	89.5
O. carteri							71.0	71.4

Measurements of comparative primate sample from ref. 29. C2, calcaneal width at sustentaculum; C3, length of posterior calcaneal facet; C4, width of posterior calcaneal facet; C5, width of calcaneo-cuboid facet; C6, height of calcaneo-cuboid facet; C8, length of distal calcaneum. 

The humeral head is rounded and extends proximally well beyond the greater and lesser tuberosities. The head is oriented proximoposteriorly (Fig. 3D) and the bicipital groove is very shallow and relatively broad. The deltopectoral crest is not well developed and the teres tubercle is only slightly better developed. Distally, the humerus of Pondaungia has a round capitulum that is separated from the trochlea by a well developed gutter (16). An entepicondylar foramen is present and the medial epicondyle is extended medially and lacks a distinct dorsoepitrochlear pit (17). The lateral epicondyle is laterally extended and the capitular tail is prominent. The olecranon fossa is relatively shallow. A large and well developed supinator crest begins at the lateral condyle and extends proximally beyond the midshaft.

The proximal ulna of Pondaungia (Fig. 4) has a moderately long olecranon process. The trochlea is relatively shallow and is angled mediolaterally. The radial articular surface is proximodistally elongate and positioned on the anterolateral surface of the ulna. The proximal shaft of the ulna just distal to the trochlea is anteroposteriorly deep and mediolaterally narrow and lacks distinct grooves for muscle attachment.

Figure 4.

(A) Composite right proximal ulna (olecranon process reconstructed from left side) of Pondaungia (NMMP 20c, 20d) in anterior view. (B) Left distal calcaneum of Pondaungia (NMMP 20e) in dorsal (Upper) and distal (Lower) views. (C) Left calcaneum of Cantius nunienus (UM 102167) in dorsal (Upper) and distal (Lower) views. Scales represent 1 cm.

The calcaneal fragment of Pondaungia (Figs. 4B and 5) preserves the distal half. The peroneal tuberosity is very small and is located proximally just plantar to the proximal calcaneal facet. The proximal calcaneal facet is relatively broad and angled plantomedially. The distal calcaneal facet (sustentacular facet) is mediolaterally narrow and extends nearly to the distal margin of the calcaneum. The calcaneocuboid articular facet is oriented dorsomedially to plantolaterally with a very deep cuboid pivot that opens plantomedially. The pit for the cuboid pivot notches the calcaneocuboid facet medially. There is a relatively large anterior plantar tubercle.

Comparisons

Comparisons of Pondaungia postcranial elements with those of selected extant and fossil primates reveals several similarities but some differences as well. In general, the proximal part of the humerus is similar to that of slow lorises (Nycticebus coucang) and some cebid platyrrhines (Cebus apella). The shape of the humeral head is rounded and broad, resembling extant Cebus but unlike Nycticebus, where the head is tapered proximally and distally. The proximal extension of the head is similar to that in extant Nycticebus (16) and North American middle Eocene notharctines (Notharctus and Smilodectes). The head extends farther proximally than in Cebus and differs from extant lemurs and Egyptian Oligocene Aegyptopithecus where the head and greater tuberosity extend nearly equidistant proximally (Fig. 3 A, B, F, and G). The head angles proximally more so than in Nycticebus, Smilodectes, or Aegyptopithecus, about as in extant Cebus, but not as much as in extant brachiators such as gibbons (Hylobates). The broad and shallow bicipital groove is similar to the condition found in lorises, lemurs, and Eocene notharctines but unlike Cebus and Aegyptopithecus where the groove is somewhat deeper. Like lorises and cebids that have reduced proximal humeral muscle attachment areas (16), the deltopectoral crest is very weak and the teres tuberosity is small. Deltopectoral crests are much stronger in extant lemurs, fossil notharctines, and some fossil anthropoids like Proteopithecus (18), Aegyptopithecus (19), and parapithecids (20).

Distally, Pondaungia humeri share less in common with lorises and cebids and are instead more similar to middle Eocene notharctine adapiforms. The rounded capitulum and the distinct gutter separating the capitulum and trochlea are found in notharctines. Platyrrhines such as Cebus and Saguinus have distinct trochlear gutters but their capitula are less rounded. The trochlea is deep medially and tapers laterally as in notharctines and Nycticebus, but differs from the more cylindrical trochlea found in omomyids and extant anthropoids. The large, rounded, distally extended capitulum of Pondaungia is shared with arboreal quadrupedal leapers such as lemurs and cheirogaleids (21). In contrast to Pondaungia, lorises have a rather flattened capitulum that is continuous with the trochlea (16). Fossil anthropoids like Catopithecus, Proteopithecus, Propliopithecus, and Aegyptopithecus have weakly rounded capitula that are continuous with the trochleae (18–19). Table 1 summarizes distal humeral measurements and indices (22) for a number of extant and fossil taxa (23, 24). Most of these indices group Pondaungia with extant arboreal quadrupeds.

The presence of an entepicondylar foramen is a primitive feature shared with a number of fossil and extant primates. Pondaungia has a relatively shallow olecranon fossa, lacks a dorsoepitrochlear pit, and possesses a strong, well developed supinator crest, features shared with notharctines and extant lemurs. Lorises have a relatively deep olecranon fossa and a relatively weak supinator crest. Extant platyrrhines like Cebus and fossil anthropoids such as Aegyptopithecus and Propliopithecus have relatively deep olecranon fossae and deep and distinct dorsoepitrochlear pits. Cebus has a reduced supinator crest whereas Aegyptopithecus and Propliopithecus have relatively strong and expanded supinator crests. Omomyids have a moderate dorsoepitrochlear pit (24) as does a distal humerus attributed to the Asian possible anthropoid Eosimias (25), but some platyrrhines (e.g., Saguinus) lack a dorsoepitrochlear pit. Catopithecus resembles Pondaungia in sharing a relatively shallow olecranon fossa but is more like other Fayum anthropoids in having a deep dorsoepitrochlear pit (18). Additionally, all of the Fayum anthropoids and most platyrrhines have strong, posteriorly angled medial epicondyles in contrast to Pondaungia where the medial epicondyle is strong but not posteriorly angled, being more similar to notharctines and extant lemurs in this characteristic.

Pondaungia has an ulnar olecranon process (Fig. 4A) comparable in relative length to that of extant lemurs and notharctine adapiforms. It is relatively much longer than in lorises and somewhat shorter than in Aegyptopithecus (26). The trochlear notch is relatively shallow as in lemurs, notharctines, and Aegyptopithecus and unlike Nycticebus where it is relatively deeper. The distal trochlea is angled medially as in lemurs and notharctines and unlike lorises and Aegyptopithecus, which have the distal trochlea aligned nearer to the long axis of the ulnar shaft. The radial articular facet is placed on the anterolateral aspect of the ulnar shaft and is flattened as in notharctines. This differs from lemurs, lorises, and Aegyptopithecus where the radial notch is more lateral and more anteroposteriorly oriented. Pondaungia has a relatively anteroposteriorly deep proximal ulnar shaft as in lemurs and Aegyptopithecus and unlike lorises and notharctines where the proximal shaft is relatively less expanded.

Among extant taxa, the distal calcaneum of Pondaungia most closely resembles lemurs, whereas among fossil taxa it is most closely comparable with adapine adapiforms (Adapis parisiensis and Adapis magnus) (Fig. 5). The distal tubercle is relatively longer in Pondaungia compared with A. parisiensis but is about as long as in A. magnus. The proximal calcaneal facet is relatively broad as in Adapis and unlike North American notharctines where it is relatively narrower. The peroneal tubercle is somewhat more robust in Pondaungia compared with Adapis but is positioned more proximally as in adapines compared with the more distal position in notharctines. The anterior plantar tubercle is relatively robust as in extant lemurs and fossil adapines, relatively larger than in notharctines.

The Pondaungia calcaneocuboid facet is different from that in lemurs and notharctines but is similar to that of Adapis, especially A. parisiensis (Table 2). The facet is oriented nearly dorsoplantarly, is relatively narrow mediolaterally, and has a very deep pit that notches the facet medially (Fig. 5). The orientation of the calcaneocuboid facet of Pondaungia is similar to that seen in Nycticebus and A. parisiensis, but the depth of the joint surface and the depth of the pit are much greater in Pondaungia.

The proximally extended and rounded humeral head of Pondaungia allows for great range of motion at the shoulder joint including above shoulder extension and adduction of the humerus (27, 28). The well developed supinator crest and the rounded capitulum indicate that the forelimb was mobile at the elbow and probably at the wrist as well. Supination is an important movement for suspension and the well developed supinator crest in Pondaungia indicates that supinator musculature was well developed (21). The shallow olecranon fossa and the moderately developed olecranon process of the ulna suggest that the arm may not have been capable of complete extension. This combination of features indicates that the forearm and arm were capable of a wide range of movements, suggesting that Pondaungia used a variety of different supports including horizontal and vertical branches and that it may have been capable of both above and below branch locomotion. The deep, rounded, and medially oriented calcaneocuboid joint indicates that great range of motion was available at the transverse tarsal joint.

The overall morphological pattern of Adapis postcrania led Dagosto (23) to interpret these fossil primates as slow-climbing arboreal quadrupeds, similar to living lorises. Although Pondaungia is similar to Adapis and Nycticebus in some morphological features, especially of the calcaneum, interpretations of other postcranial elements of Pondaungia do not provide evidence to support this interpretation. Other morphological features, especially that of the distal humerus, suggest that Pondaungia was more like fossil notharctines, primates interpreted to have been arboreal, leaping quadrupeds like extant lemurs (16, 29).

Anthropoid Status of Pondaungia

Phylogenetic implications of Pondaungia postcrania are difficult to assess. Table 3 summarizes some humeral and calcaneal comparisons of Pondaungia with some extant and extinct primate taxa. Humeral morphology is a mosaic of lorisine, cebid, omomyid, and notharctine character states with only the proximal humerus showing any unequivocally derived conditions (proximally rotated head, reduced deltopectoral crest). It is clear that Pondaungia is not closely allied with cebids or lorisines. Pondaungia has previously been aligned with notharctines on the basis of dental features (30). At present it is difficult to determine whether any of the notharctine-like features of the Pondaungia humerus are apomorphic within primates, but among the various competing hypotheses of the phylogenetic position of Pondaungia, the evidence from this element is more consistent with Pondaungia being a closer relative of notharctines than being a stem anthropoid. Recent claims of anthropoid status for Pondaungia (9) are not supported by the known postcranial evidence. Humeral and calcaneal morphology is entirely inconsistent with the hypothesis that Pondaungia is a catarrhine (6, 31, 32).

Table 3.

Morphological comparisons of Pondaungia with some extant and fossil primates

Pondaungia character	Notharctines	Fayum anthropoids	Extant lorisids	Extant cebids	Adapines	Omomyidae
Round, broad humeral head	X			X		X
Humeral head proximally extended	X		X
Humeral head proximal angle				X
Bicipital groove shallow	X		X			X
Weak deltopectoral crest			X	X
Rounded capitulum	X					X
Distinct trochlear gutter	X			X		X
Trochlear shape	X		X
Dorsoepitrochlear pit weak/absent	X		X
Strong supinator crest	X	X				X
Medial humeral condyle straight	X		X			X
Calcaneal distal tuber elongate	X					X
Proximal calcaneal facet broad					X
Peroneal tubercle proximal					X
Robust anterior plantar tubercle					X
Calcaneocuboid facet dorsoplantar			X		X

X indicates shared character state. 

The plantarly rotated, medially oriented calcaneocuboid pivot that is notched medially apparently is unique to Pondaungia, although A. parisiensis and extant lorises show similar patterns. The only postcranial character state that Pondaungia shares in common with Fayum anthropoids is a strong supinator crest, but this is also shared with notharctines.

Recent phylogenetic analyses of dental features have aligned Pondaungia and Amphipithecus with propliopithecine catarrhines (6, 31), but it is now clear that the known postcrania of Pondaungia are entirely at odds with this hypothesis. This evidence indicates to us that, unless the lineage leading to Pondaungia underwent a number of highly unlikely morphological reversals, this genus cannot be nested within the clade containing Eocene-Oligocene anthropoids from the Fayum. This, in turn, implies that the dental features aligning Pondaungia with propliopithecine catarrhines are functional convergences, for late Eocene Fayum taxa such as Proteopithecus exhibit a much more primitive dental morphotype but already exhibit typically anthropoid postcrania (18, 33) and complex anthropoid apomorphies such as postorbital closure (34). Whether the anthropoid-like dental features of Pondaungia are derived from a dental morphotype like that of notharctines, that of eosimiids, or that of primitive Paleogene Afro-Arabian anthropoids remains to be determined. Given the emerging cranial and postcranial fossil evidence from the late middle Eocene of Myanmar, however, it now appears that the possible notharctine, or at least adapiform, affinities of Pondaungia and its close relatives once again deserve serious consideration. The discovery of this associated partial skeleton draws attention to the importance of further fieldwork at the various Myanmar localities with the objective of finding combined dental, cranial, and postcranial remains that may be relevant to the question of anthropoid origins.

Abbreviations

NMMP

National Museum of Myanmar Primate

UM

University of Michigan