Jaw myology and bite force of the monk parakeet (Aves, Psittaciformes)

Abstract

Psittaciform birds exhibit novelties in jaw bone structure and musculature that are associated with strong bite forces. These features include an ossified arcus suborbitalis and the muscles ethmomandibularis and pseudomasseter. We analyse the jaw musculature of the monk parakeet (Myiopsitta monachus) to enable future studies aimed at understanding craniofacial development, morphology, function and evolution. We estimate bite force based on muscle dissections, physiological cross-sectional area and skull biomechanical modelling. We also compare our results with available data for other birds and traced the evolutionary origin of the three novel diagnostic traits. Our results indicate that, in Myiopsitta, (i) the arcus suborbitalis is absent and the orbit is ventrally closed by an elongate processus orbitalis and a short ligamentum suborbitale; (ii) the ethmomandibularis muscle is a conspicuous muscle with two bellies, with its origin on the anterior portion of the septum interorbitale and insertion on the medial aspect of the mandible; (iii) the pseudomasseter muscle consists of some fibers arising from the m. adductor mandibulae externus superficialis, covering the lateral surface of the arcus jugalis and attaches by an aponeurotic sheet on the processus orbitalis; (iv) a well-developed adductor mandibulae complex is present; (v) the bite force estimation relative to body mass is higher than that calculated for other non-psittaciform species; and (vi) character evolution analysis revealed that the absence of the arcus suborbitalis and the presence of the m. pseudomassseter are the ancestral conditions, and mapping is inconclusive about presence of one or two bellies of the m. ethmomandibularis.

Keywords: Myiopsitta monachus; ethmomandibularis muscle; evolutionary novelties; neotropical parrots; physiological cross-sectional area; pseudomasseter muscle; skull biomechanics; suborbital arch.

Figure 1

Biomechanical modelling of the jaw in Myiopsitta monachus. Two lines between the most anterior (5) and posterior (4) part of the insertion and the most posterior (1), center (2) and most anterior part (3) of the origin are drawn. The angle between the two lines is subdivided into several lines of action. All the moment arms (m1-3) are measured for each point (posterior, center and anterior) and a mean moment arm is estimated for each point. With the three moments arms, a mean moment arm is calculated. The procedure is then repeated for other muscles (input-force). See text for further explanation. Abbreviations: 1–3, most posterior, center and anterior points of the muscle origin; 4–5, most posterior and anterior edges of muscle insertion; f, fulcrum; m1-3, in-lever moment arms for the three lines between points 1 and 4 and 5; M, out-lever moment arm; out-F, out-force. Scale = 1 cm.

Figure 2

Moment arms of the m. adductor mandibulae externus profundus based on the methodology of Vizcaíno et al. (1998). A, closed beak; B, open beak. Abbreviations: m1-3, in-lever moment arm; M, out-lever. Scale bar = 1 cm. See the text for further information.

Figure 3

Jaw muscles of Myiopsitta monachus. A, C, D, lateral; B, dorso-lateral; E, cranio-lateral and F, caudal views of the skull. Abbreviations: aae, apertura auris externae; aj, arcus jugalis; AMEp, m. adductor mandibulae externus profundus; AMEs, m. adductor mandibulae externus superficialis; AMP, m. adductor mandibulae posterior; DMi, m. depressor mandibulae pars intermedia; DMp, m. depressor mandibulae pars profunda; DMs, m. depressor mandibulae pars superficialis; EM, m. ethmomandibularis; fs, fossa subtemporalis; ft, fossa temporalis; po, processus postorbitalis; PM, m. pseudomasseter; PPtQ, m. protractor pterygoideus et quadrati; ps, processus orbitalis; Pss, m. pseudotemporalis superficialis; Ptd, m. pterygoideus dorsalis; Ptv, m. pterygoideus ventralis; pz, processus zygomaticus; q, os quadratum. Scale bar = 1 cm.

Figure 4

Cranium and mandible scheme of Myiopsitta monachus. A–D, Skull; A, lateral; B, latero-caudal; C, ventral and D, cranio-lateral views. E–F, Jaw; E, detail of the medial aspect of the jaw; F, lateral view. GH, detail of the os quadratum in medial (G) and lateral (H) views. Origins are indicated in blue and insertions in red. Abbreviations: AMEp, m. adductor mandibulae externus profundus; AMEs, m. adductor mandibulae externus superficialis; AMP, m. adductor mandibulae posterior; DMi, m. depressor mandibulae pars intermedia; DMp, m. depressor mandibulae pars profunda; DMs, m. depressor mandibulae pars superficialis; EM, m. ethmomandibularis; fno, foramen nervi optici; frm, fenestra rostral mandibulae; fs, fossa subtemporalis; ft, fossa temporalis; is, septum interorbitale; pa, os palatinum; pc, processus coronoideus; PM, m. pseudomasseter; pma, processus mandibularis; pol, processus orbitalis os lacrimale; poq, processus orbitalis os quadratum; pot, processus oticus; PPtQ, m. protractor pterygoideus et quadrati; Pss, m. pseudotemporalis superficialis; pt, os pterygoideum; Ptd, m. pterygoideus dorsalis; Ptv(pa), m. pterygoideus ventralis pars palatina; Ptv(pt), m. pterygoideus ventralis pars pterygoidea; pz, processus zygomaticus. Scale bar = 1 cm.

Figure 5

Ancestral-state reconstructions of (A) arcus suborbitalis, (B) m. pseudomasseter and, (C) m. etmomandibularis in Psittaciformes based on Parsimony analysis. Phylogenetic proposal modified from Tavares et al. (2006) and Wright et al. (2008). mps, most parsimony state; *data of the extinct Nandayus vorohuensis obtained from Carril et al. (2014b).