Caenagnathidae Stenberg, 1940

Słowiak, Justyna, Brusatte, Stephen L. & Szczygielski, Tomasz, 2024, Reassessment of the enigmatic Late Cretaceous theropod dinosaur, Bagaraatan ostromi, Zoological Journal of the Linnean Society 202 (3), pp. 1-39 : 24-29

Caenagnathidae Stenberg, 1940

Referred material

ZPAL MgD-I/108/1: Left manus phalanx II-1, manus ungual I-2, proximal and distal ends of the left femur, tibiotarsus, and rib.

Note on diagnostic characters

We provide full details below, because we must first describe all the bones of the Bagaraatan original series before untangling which different taxa they belong to. However, we note here that this set of bones can be referred to Caenagnathidae because of: (i) the presence of lateral pleurocoels in the proximal caudal centra; (ii) lesser and greater trochanters in contact; (iii) clearly demarcated accessory trochanter; and (iv) gracile and straight shape of the manual phalanx.

Locality and age

Northern Sayr, Nemegt, Ömnögov, Mongolia; Nemegt Formation.

Description

Caudal vertebrae: The centrum of one caudal vertebra is preserved ( Fig. 19A–F ). It is 28 mm long, 19.5 mm tall, and 23 mm wide (the height to width ratio of the centrum is 0.8). The centrum is oval, only slightly compressed dorsoventrally. Laterally, the centrum bears one pleurocoel (pneumatic foramen) on each side. The presence of lateral pleurocoels in the caudal vertebrae is a synapomorphy of Caenagnathoidea ( Lamanna et al. 2014). The centrum is only slightly concave laterally. Ventrally, two parallel ridges extend along the centrum, as in Elmisaurus rarus (specimen MPC-D 100/119 ‘ Nomingia gobiensis ’ Barsbold et al. 2000 ).

Ribs: Only a proximal part of a dorsal rib is preserved; the rib is broken at the tuberculum ( Fig. 19G, H ). The capitulum is bulbous. Behind the slightly convex articular surface, no depression is present, in contrast to tyrannosaurids ( Ta. bataar , e.g. ZPAL MgD-I/3, ZPAL MgD-I/4, and ZPAL MgD-I/175, and Alioramus altai ; see Brusatte et al. 2012). Also, in contrast to the latter, the tuberculum is enlarged. Because the capitulum and tuberculum are at a similar level, the rib is likely to come from the posterior part of the ribcage. The overall shape of the preserved part of the rib corresponds to the morphology in caenagnathids (e.g. Caenagnathidae indet. ZPAL MgD-I/99).

Manus phalanx II-1: The left phalanx is straight and elongated, measuring 76.6 mm ( Fig. 19O–T ). The proximal articular surface is taller (18 mm) than wide (16 mm) and divided by a low ridge, which is narrow dorsally and wide ventrally. On both sides of the ridge, the articular surfaces are teardrop-shaped and strongly concave. The distal medial condyle (13.5 mm high) is smaller than the lateral one (15.4 mm high) and separated by a deep and narrow furrow. The medial ligament pit is shallower than the lateral ligament pit. The width of the distal end is 15 mm; the length to width ratio of the phalanx is 4.7.

The gracile and straight shape of the manus phalanx II-1 of ZPAL MgD-I/108/1 is the same as in Elmisaurus rarus ZPAL MgD-I/98, although the phalanx of ZPAL MgD-I/108/1 is larger. The length of manus phalanx II-1 of ZPAL MgD-I/98 is 66 mm, the proximal width 14 mm, and the distal width 12 mm (the length to width ratio is 4.7, same as for ZPAL MgDI/108/1). The manus phalanx II-1 of ZPAL MgD-I/108/1 shares also with Elmisaurus rarus slightly downturned distal condyles and expanded articular surfaces of the distal condyles. Other theropods known from the Nemegt Formation, i.e. tyrannosaurids ( Ta. bataar , e.g. ZPAL MgD-I/3 and ZPAL MgD-I/4), ornithomimids ( Ga. bullatus , cast of MPC-D 100/11; Deinocheirus mirificus Osmólska & Roniewicz, 1970, cast of MPC-D 100/18), avimimids [alvarezsaurids ( Mononykus olecranus Perle et al., 1993 (Perle et al. 1994)], and oviraptorids [e.g. Oksoko avarsan ( Funston et al. 2020a) , Nemegtomaia barsboldi Lu et al., 2005 (Fanti et al. 2012)] do not have manual phalanges that are so straight, slender, and elongated.

Manus ungual II-3: The ungual is elongated (54 mm in length), curved, and very narrow, and the proximal articular surface is 13 mm wide ( Fig. 19I–N ). The ungual lacks only the distal tip. The proximal articular surface is oval (longer dorsoventrally than mediolaterally). A vertical ridge, which is dorsally and ventrally expanded but constricted in the middle section, extends across the middle of the articular surface. The articular surfaces on both sides of the ridge are strongly concave. The dorsal edge of the articular surface forms a robust dorsal lip, surrounded by a depression. A ventral process is present on the ventral edge of the articular surface. The articular surface is separated by a notch from the ventrodistally located enlarged flexor tubercle. Laterally and medially, the collateral groove extends along the entire ungual, starting from the area above the flexor tubercle.

The manus ungual II-3 is not known in Elmisaurus rarus ; however, the presence of the distinctive dorsal lip indicates that the ungual corresponds to the manual unguals of Caenagnathidae . In comparison to the manual unguals of an North American caenagnathid, Chirostenotes pergracillis Gilmore, 1924 , CMN 2367 ( Funston 2020), the ungual of ZPAL MgD-I/108/1 is less curved than the phalanges I-2 and III-4, but more straight, similar to II-3. Moreover, the proximal articulation is offset, and the flexor tubercle is distally positioned and smaller in contrast to unguals I-2 and III-4, which further supports its identification as II-3 of a caenagnathid. Other theropods known from the Nemegt Formation, i.e. tyrannosaurids ( Ta. bataar , e.g. ZPAL MgD-I/3 and ZPAL MgD-I/4), ornithomimids ( Ga. bullatus , cast of MPC-D 100/11; De. mirificus , cast of MPC-D 100/18), alvarezsaurids [ M. olecranus (Perle et al. 1994) ], and oviraptorids [ O. avarsan ( Funston et al. 2020a) and N. barsboldi (Fanti et al. 2012) ] do not have such enlarged, curved, and transversely narrow manual unguals with an enlarged flexor tubercle distinctly separated from the ventral process and distinctive dorsal lip.

Femur: Two parts of the left femur are preserved: the proximal and distal end; most of the shaft is missing, hence the length of the femur is unknown ( Fig. 20 ). The circumference of the shaft portions preserved with the distal and proximal parts is 105 mm. Osmólska (1996) hypothesized that ~ 80–90 mm of the shaft is missing, adding up to a total femur length of 310–320 mm.

The proximal part of the femur ( Fig. 20A–E ) is narrower lateromedially than longer anteroposteriorly. In dorsal view, the femur is L-shaped. The posterior part of the greater trochanter is connected to the femoral head that projects mediodistally, and the anterior part of the greater trochanter is widened anteriorly. In anterior view, the femoral head is positioned higher than the greater trochanter, and they are separated by a broad, shallow depression. The surface of the rounded femoral head is rugose. In posterior view, a wide groove for the capital ligament is present on the femoral head. In medial view, the femoral head is ovoid, and its posterodorsal margin is wider than the anteroventral end. The neck is narrower anteroposteriorly than the head; and the ventral margin of the head is directed downwards before connecting to the neck. The neck extends upwards from the greater trochanter, which is wider lateromedially than the lesser trochanter. The lesser trochanter is almond-shaped in anterior view. The dorsal margin of the femoral trochanters in lateral view is arched; the small, anteriorly positioned lesser trochanter is separated by a shallow groove from the much anteroposteriorly longer greater trochanter. On the lateral surface of the proximal part of the femur, the separation between the lesser and greater trochanter is marked by a shallow and short groove. Below the lesser trochanter, the accessory trochanter (anterior crest sensu Osmólska 1996) is present. It is slightly expanded anteriorly and extends along the preserved part of the proximal shaft. The accessory trochanter keeps a consistent lateromedial width along the preserved proximal part of the shaft. A posterior tubercle is present below the greater trochanter, well visible in anterior and posterior views.

The distal end of the femur is now longitudinally shorter than described by Osmólska (1996), because it has since been thin sectioned. At that time, it measured 105 mm; now, only the distalmost part of the femur including both condyles is present, measuring 52 mm ( Fig. 20F–J ). The medial condyle is bigger than the lateral condyle, but the lateral condyle extends further distally than the medial condyle. The condyles are distally separated by a deep but narrow notch (the popliteal fossa). Anteriorly and distally, the condyles are separated by shallower and wider depressions (the extensor grooves). The medial condyle is convex, with a slightly rugose surface. The lateral condyle bears an elevation on its distal surface. The tibiofibular crest extends posteromedially. In lateral view, the tibiofibular crest is axeshaped and projects further posteriorly than the medial condyle.

The accessory trochanter appeared in Tetanurae as a branch of the distal base of the lesser trochanter, and it was reduced in Eumaniraptora. The accessory trochanter is smaller in basal Tetanurae, Carnosauria, basal Coelurosauria, Tyrannosauridae, and Ornithomimosauria than in Caudipteryx spp. , Microvenator celer Ostrom, 1970 , Caenagnathidae , and some Oviraptoridae ( Hutchinson 2001) . The accessory trochanter of the femur of ZPAL MgD-I/108/1 is clearly demarcated from the lesser trochanter and forms a dorsoventral flange, comparable to that seen in Caenagnathidae , e.g. Elmisaurus rarus ZPAL MgD-I/98, Anzu oyliei Lamanna et al., 2014 , or Chirostenotes pergracilis Gilmore, 1924 (Currie and Russell 1987). The lesser and greater trochanters are in contact, as in all Caenagnathoidea ( Lamanna et al. 2014). The proximal end of the femur further resembles the femur of Elmisaurus rarus ZPAL MgD-I/ 98 in possessing a cylindrical head positioned higher than the greater trochanter and separated by a depression, which is wider in the larger (ontogenetically older, as indicated by the difference in size between those specimens) ZPAL MgD-I/108/1. Such an embayment is also present in other Caenagnathidae , e.g. Anzu oyliei (see Lamanna et al. 2014), Elmisaurus rarus (see Barsbold et al. 2000), or Ch. pergracilis (see Currie and Russell 1987). A wide groove on the posterior surface of the femoral head for the capital ligament is present in both Elmisaurus rarus ZPAL MgD-I/98 and MgDI/108/1. Also, similar to Caenagnathidae , the lateral condyle of the femur ZPAL MgD-I/108/1 is positioned more distally than the medial condyle, and the tibiofibular crest is well demarcated [ Anzu oyliei (see Lamanna et al. 2014), Elmisaurus rarus (see Barsbold et al. 2000), or Ch. pergracilis (see Currie and Russell 1987)]. The extensor groove is distinct, but shallow, consistent with Elmisaurus rarus (see Barsbold et al. 2000). The proximal and distal ends of the femur ZPAL MgD-I/108/1 are of similar size to the measurements in Elmisaurus rarus (see Barsbold et al. 2000), hence the probable length of the whole bone was similar, ~ 285 mm.

Bone microstructure of femur: A histological section of the distal part of the shaft, above the condyles, shows a large marrow cavity and thin (~ 2 mm) cortex ( Fig. 20K, L ). The external part of the cortex (half of its thickness) is built of parallel-fibred bone, with scattered secondary osteons. The vascularization is laminar, and growth marks are absent. In the section, no definite primary osteons were seen, although the external cortex is poorly preserved, possibly obscuring their presence. The inner cortex is sharply demarcated from the external cortex and built of densely packed secondary osteons: up to four generations are present. Close to the marrow cavity, resorption cavities are present, surrounded by a thick layer of lamellar bone (≤ 0.3 mm). The marrow cavity is surrounded by a thinner layer of lamellar bone (0.15 mm) and filled by slender and elongated bony trabeculae.

The section shows features typical for the metaphyses of long bones: extensive secondary remodelling, lack of growth marks, and numerous resorption cavities. Thus, owing to the lack of any growth record in the section, it is not possible to estimate the growth ratio.

The bone microstructure of the femur in caenagnathids is unknown. Thus far, bone histology of the tibiae of cf. Anzu oyliei (ROM 65884) and Caenagnathidae indet. (UALVP 57349) have been described ( Funston and Currie 2018, Cullen et al. 2021). Both, however, represent young individuals, as indicated by their predominant fibrolamellar bone, high vascularity, and limited secondary remodelling (none in UALVP 57349 and ≤ 30% of cortex in OMVP 65884). The predominance of fibrolamellar bone and high vascularity are also seen in the cortices of the femora and fibulae of the oviraptorid O. avarsan , regardless of their ontogenetic age ( Funston et al. 2020a). Even in the large-bodied cf. Anzu oyliei (ROM 65884), the section from the tibia revealed a predominately primary tissue, with generally high vascularity and limited secondary remodelling ( Cullen et al. 2021). As can be noticed, the section taken from ZPAL MgD-I/108/1 is different from the Caenagnathoidea described before, which is a result of its sectioning at the metaphysis, and not the diaphysis as usually done.

Tibiotarsus: The left tibiotarsus is complete and measures 380 mm ( Fig. 21A–F ). The bone is slender, slightly bowed laterally (possibly taphonomically exaggerated), and the distal fibula is fused to the distal tibia and calcaneum ( Fig. 21A–C ). The shaft is elliptical in cross-section (circumference 95 mm) and is compressed anteroposteriorly, possibly as an effect of taphonomical crushing. Proximally, the tibia expands anteriorly and slightly mediolaterally; its anteroposterior depth is 47.5 mm and mediolateral width 59.2 mm. Distally, where the tibia is fused with the astragalocalcaneum distally and the fibula laterally, the tibia expands mediolaterally and measures 57.3 mm.

The cnemial crest condyle (cranial cnemial crest sensu Osmólska 1996) is robust, laterally deflected, and short in anterior view, comprising only ~15% of the maximum proximodistal tibiotarsus length. The fibular condyle (lateral cnemial crest sensu Osmólska 1996) is also robust, slightly curved anteriorly, and shorter mediolaterally and dorsoventrally than the cnemial crest. Between the cnemial crest and fibular condyle, a deep and posteriorly curved incisura tibialis is present ( Fig. 21A–E ). The medial proximal condyle of the tibiotarsus is long anteroposteriorly; anteriorly, it is smoothly connected with the cnemial crest; posteriorly, it is separated from the fibular condyle by a triangular cleft. The posteromedial edge of the medial proximal condyle of the tibiotarsus is posteriorly extended. Below the fibular condyle, the fibular crest is present. It is tall dorsoventrally, ~20% of the tibiotarsus length. The crest becomes wider mediolaterally and deflects anteriorly; however, the crest is not strongly pronounced. The distal end of the crest is rectangular.

The fibula is fused to the lateral side of the distal end of the tibia, along the distal ~ 23% of the tibiotarsus length ( Fig. 21A–C ). The distal end of the fibula is partly fused with the calcaneum. The outline of the distal part of the fibula is marked and distinguishable against the remaining bones. The suture between the astragalocalcaneum and distal tibia are clearer in anterior than posterior view; however, that might be a matter of preservation. No suture is visible between the astragalus and calcaneum. The calcaneum shows a lateral depression (lateral epicondylar depression) below the suture with the fibula. The preserved, incomplete ascending process of the astragalus extends along 7.5% of the length of the tibiotarsus. In anterior view, it has subtriangular, pointed medial and lateral processes, separated by a deep depression. At the base of the ascending process, a shallow median depression is present, above which a low, mediolaterally extended ridge is located ( Fig. 21A ).

A proper tibiotarsus, in which the tibia is fused to the proximal tarsals, is recognized in three non-avian maniraptoran taxa: Alvarezsauridae, Troodontidae, and Avimimidae. Both alvarezsaurids known from the Nemegt Formation (M. olecranus and Nemegtonykus citus Lee et al., 2019 ) have a proximodistally short fibula, which does not reach even the midshaft of the tibiotarsus (Perle et al. 1994, Lee et al. 2019). The presence of a tibiotarsus in the troodontids known from the Nemegt Formation is variable. In the larger species Zanabazar junior ( Barsbold, 1974) , the astagalocalcaneum is not fused to the tibia ( Norell et al. 2009), whereas in the smaller Bo. gracilicrus , a tibiotarsus is present (Osmólska 1987, Cau and Madzia 2021). The hindlimb is unknown in the third troodontid from the Nemegt Formation, Tochisaurus nemegtensis Kurzanov & Osmólska, 1991 . Only a fragment of proximal right fibula of Bo. gracilicrus is preserved, but the distal end of the tibiotarsus does not show any signs of fusion with the distal fibula, as in other Troodontidae (e.g. Gao et al. 2012). Oviraptoridae and Caenagnathidae show a fused astragalus and calcaneum, but not to the tibia ( Currie et al. 2016). Finally, a fused tibiotarsus including the distal end of the fibula is an autapomorphy of Avimimus spp. ( Kurzanov 1981, Funston et al. 2018).

However, ZPAL MgD-I/108/1 would be an exceptionally large representative of Avimimus ; the largest reported tibiotarsus of Avimimus nemegtensis Funston, Mendonca, Currie & Barsbold, 2018 MPC-D 102/92 measures 282 mm ( Funston et al. 2016), and in Avimimus portentosus Kurzanov, 1981 PIN 3907/1 it is 257 mm long ( Kurzanov 1981), whereas ZPAL MgD-I/108/1 measures 380 mm, similar to Elmisaurus rarus MPC-D 100/119, i.e. 355 mm. The histological sections of the Iren Dabasu avimimids revealed that the largest sectioned specimens were already adults (Funston et al. 2019). Moreover, three features of the tibia are shared by ZPAL MgD-I/108/1 and Elmisaurus rarus : (i) the medial proximal condyle is more protruded dorsally than in Avimimus spp. ; (ii) the fibular crest is longer, and its distal end is rectangular, not arcuate as in Avimimus spp. ; and (iii) the medial malleolus protrudes further medially than in Avimimus spp.

Fibula: The left fibula is complete, measuring 340 mm. The distal end is partly fused to the calcaneum and laterally fused to the tibia, along ~33% of the length of the fibula. It is similar to Avimimus portentosus , in which the fibula is fused to the tibia along onethird of its length ( Kurzanov 1981). The proximal anteroposterior length of the fibula is 47.1 mm. The proximal end of the fibula is triangular in the lateromedial aspect, only slightly concave medially in dorsal view ( Fig. 21G–K ), similar to Elmisaurus rarus (MPC-D 100/119; Barsbold et al. 2000) and in contrast to the rectangular proximal end in Avimimus spp. ( Kurzanov 1981, Funston et al. 2016). Distal to the expanded proximal end, the fibula narrows anteroposteriorly. On the medial surface is a long (74.2 mm, ~22% of total length) fusiform attachment for the fibular crest of the tibia. At this level, on the anterior surface of the fibula, an elliptical iliofibularis tubercle is present. Distally, the fibula strongly narrows anteroposteriorly and has a triangular cross-section along ~65% of its total length.

Despite the distal part of fibula being fused with the tibia in a similar manner to Avimimus spp. , the proximal end of the fibula is more triangular, as in MPC-D 100/119 (Barsbold et al. 2000), than rectangular, as seen in Avimimus spp.

Pedal phalanx: The left phalanx II-2 is 35 mm long ( Fig. 19 U-A ʹ), and its length to width ratio is two. The proximal articular surface is triangular in posterior view and can be divided into lateral and medial teardrop-shaped concave articular surfaces, separated from each other by a smooth ridge running in the middle of the proximal articular surface. In the lateral and medial views, the proximal articular surface is strongly concave, the plantar margin extends backwards, and the lip-shaped dorsal margin (extensor turbecle) is elevated dorsally and directed posteriorly. The distal articular surface is composed of the lateral condyle and slightly shorter plantodorsally medial condyle, which are separated by a concavity that is shallow dorsally but becomes deeper along the articular surface to its end on the plantar side. In anterior view, the lateral condyle extends further downwards than the medial condyle. The ligament pits are well marked on the both sides of the phalanx; the lateral ligament pit is elongated anteroposteriorly, and the medial ligament pit is circular.

The phalanx II-2 is similar to the corresponding phalanx of Elmisaurus rarus (ZPAL MgD-I/98; length to width ratio of 2.1), especially in the structure of the proximal articular surface, i.e. two teardrop-shaped surfaces separated by a ridge, and the lip-like extensor tubercle. The phalanx II- 2 in other theropods from the Nemegt formation differs from the one of ZPAL MgD-I/108/1. This phalanx in Ga. bullatus (ZPAL MgD-I/94) is compressed (the length to width ratio is 1.4), and the extensor tubercle is less pronounced than in ZPAL MgD-I/108/1. The phalanx II-2 is even more compressed in Bo. gracilicrus (ZPAL MgD-I/174; the length to width ratio is 1.2). The proximal articular surface in Ta. bataar (ZPAL MgD-I/3, ZPAL MgD-I/4, ZPAL MgD-I/29, and ZPAL MgD-I/175) is wider than long, in contrast to Elmisaurus rarus , Ga. bullatus , and ZPAL MgDI/108/1. The length to width ratio of the phalanx II- 2 in Ta. bataar is 1.5–1.6, depending on the ontogenetical age.

Figures

Figure 19. Various bones of Caenagnathidae indet. ZPAL MgD-I/108/1. A–F, caudal vertebra in anterior (A), left lateral (B), posterior (C), right lateral (D), dorsal (E), and ventral (F) view. G, H, proximal part of dorsal rib. I–N, manus ungual II-3 in dorsal (I), medial (J), ventral (K), lateral (L), anterior (M), and posterior (N) view.O–T, left manus phalanx II-1 in medial (O), ventral (P), lateral (Q), dorsal (R), anterior (S), and posterior (T) view.U–Aʹ, left pedal phalanx II-2 in medial (U), ventral (W), lateral (X), dorsal (Y), anterior (Z), and posterior (Aʹ) view.

Figure 20. Left femur of Caenagnathidae indet. ZPAL MgD-I/108/1. A–E, proximal end of the femur in anterior (A), lateral (B), posterior (C), medial (D), and dorsal (E) view.F–J, distal end of the femur in anterior (F), lateral (G), posterior (H), medial (I), and ventral (J) view.K, L, thin section of the femoral cortex under polarized light. Red arrows indicate secondary osteons; green arrows point to resorption cavities; yellow arrows indicate lamellar bone; and purple arrows point to parallel-fibred bone.

Figure 21. Left tibiotarsus of Caenagnathidae indet. ZPAL MgD-I/108/1. A–F, tibiotarsus in anterior (A), lateral (B), posterior (C), medial (D), dorsal (E), and ventral (F) view. G–K, proximal fibula in dorsal (G), anterior (H), lateral (I), posterior (J), and medial (K) view.