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, 7 (4), e31556

Anatomy and Cranial Functional Morphology of the Small-Bodied Dinosaur Fruitadens Haagarorum From the Upper Jurassic of the USA

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Anatomy and Cranial Functional Morphology of the Small-Bodied Dinosaur Fruitadens Haagarorum From the Upper Jurassic of the USA

Richard J Butler et al. PLoS One.

Abstract

Background: Heterodontosaurids are an important but enigmatic and poorly understood early radiation of ornithischian dinosaurs. The late-surviving heterodontosaurid Fruitadens haagarorum from the Late Jurassic (early Tithonian) Morrison Formation of the western USA is represented by remains of several small (<1 metre total body length, <1 kg body mass) individuals that include well-preserved but incomplete cranial and postcranial material. Fruitadens is hypothesized to represent one of the smallest known ornithischian dinosaurs.

Methodology/principal findings: We describe the cranial and postcranial anatomy of Fruitadens in detail, providing comparisons to all other known heterodontosaurid taxa. High resolution micro-CT data provides new insights into tooth replacement and the internal anatomy of the tooth-bearing bones. Moreover, we provide a preliminary functional analysis of the skull of late-surviving heterodontosaurids, discuss the implications of Fruitadens for current understanding of heterodontosaurid monophyly, and briefly review the evolution and biogeography of heterodontosaurids.

Conclusions/significance: The validity of Fruitadens is supported by multiple unique characters of the dentition and hindlimb as well as a distinct character combination. Fruitadens shares highly distinctive appendicular characters with other heterodontosaurids, strengthening monophyly of the clade on the basis of the postcranium. Mandibular morphology and muscle moment arms suggest that the jaws of late-surviving heterodontosaurids, including Fruitadens, were adapted for rapid biting at large gape angles, contrasting with the jaws of the stratigraphically older Heterodontosaurus, which were better suited for strong jaw adduction at small gapes. The lack of wear facets and plesiomorphic dentition suggest that Fruitadens used orthal jaw movements and employed simple puncture-crushing to process food. In combination with its small body size, these results suggest that Fruitadens was an ecological generalist, consuming select plant material and possibly insects or other invertebrates.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Cranial reconstruction of Fruitadens haagororum.
Fragments representing cranial and mandibular material preserved in LACM 115747 and 128258 are superimposed on the preserved skull of Tianyulong confuciusi (shown in gray). Outline of posterior cranium, extrapolated from Heterodontosaurus tucki, shown by dotted lines.
Figure 2
Figure 2. Fruitadens haagarorum, LACM 115747 (holotype), left maxilla.
Maxilla in lateral (A, C, E), medial (B, D, F), ventral (G, I, K), and dorsal (H, J, L) views, with photographs (A, B, G, H), external renderings from μCT data (C, D, I, J), and reconstructions from μCT data (E, F, K, L). See also video S1. Elements in the CT reconstructions are colour-coded as follows: maxilla, blue; functional teeth, yellow; replacement teeth, orange; internal canals, red; palatal (vomer?) fragment, green. Asterisks mark the position of the transverse μCT cross section in Figure 3. Abbreviations: antf, antorbital fossa; asc, broken base of ascending process; dia, diastema between premaxilla and maxilla; for, foramen; mxsh, maxillary shelf.
Figure 3
Figure 3. Fruitadens haagarorum, LACM 115747 (holotype), μCT data for the dentition of the left maxilla.
Reconstructed dentition (surrounding bone removed) in lateral (A), medial (B), and posteromedial (C) views. Reconstructed posterior replacement tooth in medial view (D), and reconstructed anterior replacement tooth in anteromedial view (E). External renderings of crowns 5 and 6 in lateral view (F). Transverse (G) and longitudinal (H) μCT cross sections through maxilla (see asterisks in Figure 2A for the position of the transverse cross section) showing the spongy bone surrounding the tooth roots. Elements in the CT reconstructions are colour-coded as follows: functional teeth, yellow; replacement teeth, orange. Abbreviation: rec, replacement crown. Numbers indicate tooth positions from anterior to posterior.
Figure 4
Figure 4. Fruitadens haagarorum, LACM 115747 (holotype), right dentary.
Dentary in lateral (A, C, E), medial (B, D, F), and dorsal (G, I, J) views, with photographs (A, B, G), external renderings from μCT data (C, D, I), and reconstructions from μCT data (E, F, J). Reconstructed and extracted dentition in medial view (H). Close-up of the reconstructed and extracted posterior replacement teeth in lateral view (K). Close-up of the external rendering showing the symphyseal region in medial view (L). Longitudinal CT slice (M) through the entire element and sagittal CT slice (N) through the anterior part of the mandible. See also video S2. Elements in the CT reconstructions are colour-coded as follows: dentary, blue; functional teeth, yellow; replacement teeth, orange; internal canals, red. The dentary has been made transparent in order to better visualize its internal anatomy. Abbreviations: 1pc, position of the ‘pre-caniniform’ (missing in this specimen); 2can, caniniform tooth in second tooth position; adf, anterior dentary foramen; con, concavity dorsal to the symphyseal surface; for, foramina; mc, mandibular canal within the dentary; mgr, Meckelian groove; rec, replacement crown; rfor, replacement foramen; sym, symphyseal surface; syri, curved ridge marking dorsal margin of symphysis. Numbers indicate tooth positions from anterior to posterior.
Figure 5
Figure 5. Fruitadens haagarorum, LACM 128258, right dentary.
Dentary in lateral (A, C, E), medial (B, D, F), dorsal (G, I), and ventral (H, J) views, with photographs (A, B, G, H), external renderings from μCT data (C, D), and CT reconstructions from μCT data (E, F, I, J). Reconstructed and extracted dentition in lateral (K) and medial (M) views. Photograph of the dentary in lateral view by PMG in the 1980s before the caniniform was damaged and lost (L). Photograph of a cast of the maxilla and left and right dentaries of LACM 128258 as originally preserved (N). See also video S3. Elements in the CT reconstructions are colour-coded as follows: dentary, blue; functional teeth, yellow; replacement teeth, orange. The dentary has been made transparent in order to better visualize its internal anatomy. Abbreviations: 1pc, ‘pre-caniniform’; 2can, caniniform tooth in second tooth position; mgr, Meckelian groove; rec, replacement crown. Numbers indicate tooth positions from anterior to posterior.
Figure 6
Figure 6. Fruitadens haagarorum, LACM 128258, left dentary.
Dentary in lateral (A, C, E), medial (B, D, F), and dorsal (G, H, I) views, with photographs (A, B, G), external renderings from μCT data (C, D, H), and CT reconstructions from μCT data (E, F, I). Reconstructed and extracted dentition in lateral (J) and medial (K) views. Elements in the CT reconstructions are colour-coded as follows: dentary, dark blue; fragment of coronoid, light blue; functional teeth, yellow; replacement teeth, orange. The dentary has been made transparent in order to better visualize its internal anatomy. Abbreviations: 2can, caniniform tooth in second tooth position; rec, replacement crown. Numbers indicate tooth positions from anterior to posterior.
Figure 7
Figure 7. Fruitadens haagarorum, cranial bones.
LACM 128258, right premaxilla in ventral (A) and lateral (B) views. LACM 128258, partial left maxilla, μCT slice (C), and ventral (D), lateral (E, G), and medial (F, H) views, as photographs (E, F) and reconstruction from μCT data (D, G, H). LACM 128303, partial left dentary in lateral (I) and medial (J) views. Elements in the CT reconstructions are colour-coded as follows: maxilla, blue; functional teeth, yellow; replacement teeth, orange. The maxilla has been made transparent in order to better visualize its internal anatomy. Abbreviations: 2can, position of the caniniform tooth (missing); lpm, left premaxilla; rc, replacement crown; rpmp, right premaxillary palate; sym, dentary symphysis. Numbers indicate tooth positions from anterior to posterior.
Figure 8
Figure 8. The post-caniniform (“cheek") tooth rows of various heterodontosaurid genera.
Anterior end of the tooth row is always to the left (some images have been flipped horizontally). Areas of breakage are shaded in gray. A. Fruitadens haagarorum (holotype, LACM 115747), left maxillary teeth in labial view. B. Fruitadens haagarorum (LACM 128258), right dentary teeth in lingual view. C. Echinodon becklesii (NHMUK OR 48211), right maxilla in labial view (image has been flipped horizontally). D. Echinodon becklesii (NHMUK OR 48213), left dentary in lingual view (image has been flipped horizontally). E. Abrictosaurus consors (NHMUK RU B54), left maxillary and dentary (partially obscured) tooth rows in labial view. F. “Lanasaurus scalpridens" (BPI 4244), left maxillary teeth 2–8 in labial view. G. Heterodontosaurus tucki (SAM-PK-K1332), left maxillary teeth 2–8 in labial view. H. Heterodontosaurus tucki (SAM-PK-K1332), right dentary teeth 3–11 in lingual view.
Figure 9
Figure 9. Fruitadens haagarorum, LACM 115747 (holotype), cervical and dorsal vertebrae.
Anterior cervical vertebra in left lateral (A), anterior (B), ventral (C) and posterior (D) views. Posterior cervical centrum in left lateral (E) and ventral (F) views. Anterior dorsal centrum in right lateral (G) and anterior (H) views. Dorsal vertebra in anterior (I), lateral (J) and ventral (K) views. Posterior dorsal centrum in lateral (L) and ventral (M) views. Abbreviations: dia, diapophysis; ke, keel; pa, parapophysis; pro, ventral projection.
Figure 10
Figure 10. Fruitadens haagarorum, LACM 115747 (holotype), sacral vertebrae.
First sacral vertebra in left lateral (A), ventral (B), anterior (C), and posterior (D) views. Sacral vertebrae 2–4 in left lateral (E), anterior (F), and ventral (G) views. Sacral vertebrae 5 and 6 in posterior (H), left lateral (I) and ventral (J) views.
Figure 11
Figure 11. Fruitadens haagarorum, LACM 115747 (holotype), caudal vertebrae.
Anterior caudal vertebrae in left lateral (A, D, F), anterior (B, G), and dorsal (C, E) views. Distal caudal vertebrae in left lateral view (H, I). Abbreviations: poz, postzygapophysis; prz, prezygapophysis; tvp, transverse process.
Figure 12
Figure 12. Fruitadens haagarorum, LACM 120478, left humerus.
Humerus in posterior (A) medial (B), anterior (C), lateral (D), proximal (E) and distal (F) views. Left humerus as originally preserved, prior to damage to the deltopectoral crest (photographs taken by PMG). Abbreviations: dpc, deltopectoral crest; gr, groove on proximal surface; he, head; mtub, medial tubercle; rcon, radial condyle; ucon, ulnar condyle.
Figure 13
Figure 13. Fruitadens haagarorum, femoral anatomy.
LACM 115747 (holotype), proximal right femur in anterior (A), lateral (B), posterior (C), medial (D) and proximal (E) views. LACM 115727, proximal right femur in anterior (F), lateral (G), posterior (H), medial (I) and proximal (J) views. Note that only the proximal portion of the shaft is shown; more distal parts are preserved, but it is not clear if they have been reconstructed correctly. LACM 115727, cross section through the femur at approximately mid-length (K). LACM 120478, distal left femur in anterior (L), lateral (M), posterior (N), medial (O), cross-sectional (at preserved proximal end: P) and distal (Q) views. LACM 120478, sketch of the midshaft of the left femur as preserved in the 1980s, prior to damage to the fourth trochanter (modified from Callison & Quimby 1984). Abbreviations: atr, anterior trochanter; ftr, fourth trochanter; gr, transverse groove on distal femur; lpd, broad depression on lateral surface of greater trochanter; nt, shallow notch separating proximally the greater and anterior trochanters; ppr, subtle posterior projection of femoral head; pr, small knob-like projection on posterior surface of proximal end; tri, thickened ridge delimiting the posterior margin of the greater trochanter.
Figure 14
Figure 14. Fruitadens haagarorum, distal hindlimb.
LACM 120478, articulated left tibia, fibula and astragalocalcaneum in anterior (A), medial (B), posterior (C), lateral (D), proximal (E) and distal (F) views. LACM 115747 (holotype), proximal left tibia in lateral (G) and medial (H) views. LACM 115727, distal left tibia with attached astragalocalcaneum in anterior (I), medial (J), posterior (K), lateral (L) and distal (M) views. LACM 115747 (holotype), distal right tibia in distal (N) and anterior (O) views. LACM 120602, left astragalocalcaneum in anterior (P) and proximal (Q) views. Abbreviations: amsh, anteromedial sheet of tibia; asp, ascending process; cal, calcaneum; cnc, cnemial crest; fibc, fibular condyle; for, foramen; innc, inner condyle; int, notch between inner condyle and fibular condyle.
Figure 15
Figure 15. Fruitadens haagarorum, line drawings of distal hindlimb.
LACM 120478, articulated left tibia, fibula and astragalocalcaneum in anterior (A), medial (B), posterior (C), and lateral (D) views. LACM 115727, distal left tibia with attached astragalocalcaneum in anterior (E), medial (F), posterior (G), and lateral (H) views. Abbreviations: amsh, anteromedial sheet of tibia; ast, astragalus; cal, calcaneum; cnc, cnemial crest; dasp, dorsal part of ascending process, formed by separate ossification; fib, fibula; fib.a, articular surface for fibula; fibc, fibular condyle; for, foramen; innc, inner condyle.
Figure 16
Figure 16. Fruitadens haagarorum, LACM 120602, metatarsals and pedal phalanges.
Left metatarsal I in dorsal view (A). Right metatarsal I in lateral view (B). Additional metatarsal (position uncertain) in dorsal (C) and medial or lateral (D) views. Phalanx I-1 in lateral or medial view (E). Phalanx (position uncertain) in dorsal view (F). Phalanx III-1 in lateral or medial (G) and dorsal (H) views.

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