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The Avian Lingual and Laryngeal Apparatus Within the Context of the Head and Jaw Apparatus, with Comparisons to the Mammalian Condition: Functional Morphology and Biomechanics of Evaporative Cooling, Feeding, Drinking, and Vocalization

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The Biology of the Avian Respiratory System

Abstract

The lingual and laryngeal apparatus are the mobile and active organs within the oral cavity, which serves as a gateway to the respiratory and alimentary systems in terrestrial vertebrates. Both organs play multiple roles in alimentation and vocalization besides respiration, but their structures and functions differ fundamentally in birds and mammals, just as the skull and jaws differ fundamentally in these two vertebrate classes. Furthermore, the movements of the lingual and laryngeal apparatus are interdependent with each other and with the movements of the jaw apparatus in complex and little-understood ways. Therefore, rather than updating the existing numerous reviews of the diversity in lingual morphology of birds, this chapter will concentrate on the functional-morphological interdependences and interactions of the lingual and laryngeal apparatus with each other and with the skull and jaw apparatus. It will:

  1. 1.

    Briefly review the salient features of the mammalian head as a baseline against which to understand the uniqueness of the avian head

  2. 2.

    Describe general morphological features of the lingual and laryngeal apparatus within the context of the skull and jaw apparatus

  3. 3.

    Contrast some fundamental functional-morphological differences that exist among the jaw, lingual and laryngeal apparatus of birds

  4. 4.

    Provide models of the movements of the various parts of the lingual and laryngeal apparatus based on biomechanical analyses

  5. 5.

    Integrate these models with behaviors in thermoregulation, feeding, drinking, and vocalization

  6. 6.

    Briefly demonstrate how detailed morphological and functional analyses can be tested and expanded by using 3D visualization and animation

  7. 7.

    Place the provided data in an evolutionary framework

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Notes

  1. 1.

    The term akinetic for the mammal skull originated at a time when it was believed that the skull, excluding the lower jaw, was a rigid entity. Since then it has been increasingly understood that the sutures between the individual cranial and facial bones provide significant flexibility, which is necessary not only for the growth and maintenance of the cranial bones but also for balancing the forces that are exerted on the skull during mastication (see, e.g., Herring and Teng 2000).

  2. 2.

    Besides the joints of the incus with the stapes and malleus in the middle ear.

  3. 3.

    For a discussion of the capacity for articulated speech in adult humans, see Sect. 2.9.

  4. 4.

    The anatomical terms follow the Nomina Anatomica Avium (Baumel et al. 1993); hence, oral cavity (cavum oris) is used for what recent physiological-experimental papers have termed “oropharyngeal” or “oropharyngeal-esophageal” cavity (for a review, see Riede et al. 2013).

  5. 5.

    The adult upper beak is formed from various embryonic elements (for details, see Bühler 1981).

  6. 6.

    The exact place and structure of this joint varies among birds (for details, see Bühler 1981).

  7. 7.

    The “seed cup” described by Heidweiller and Zweers (1990) is a different structure between the tip of the fleshy tongue and a rostral projection of the lingual nail.

Abbreviations

Al.ling:

Ala linguae

Al.lingc:

Ala linguae caudalis

Al.lingr:

Ala linguae rostralis

Ap.ling:

Apex linguae

AR:

Arytenoideum

AR.cart:

Cartilaginous portion of the Arytenoideum

Ar.prgl:

Area preglottalis, lingual base (Zweers and Berkhoudt 1987)

Art.:

Articulatio, joint

Art.ar:

Art. intra-arytenoidea

Art.cb:

Art. cerato-basihyalis

Art.cf:

Art. craniofacialis

Art.crp:

Art. crico-procricoidea

Art.ecb:

Art. epi-ceratobranchialis

Art.eph:

Art. epi-pharyngobranchialis

Art.icr:

Art. intracricoidea

Art.icrd:

Art. intracricoidea dorsalis

Art.icrdv:

Art. intracrioidea ventrodorsalis

Art.jr:

Art. jugo-rostralis

Art.par:

Art. processo-arytenoidea

Art.pgb:

Art. paraglosso-basihyalis

Art.ppr:

Art. pterygo-palatorostralis

Art.pr:

Art. palato-rostralis

Art.pra:

Art. procrico-arytenoidea

Art.qj:

Art. quadrato-jugalis

Art.qm:

Art. quadrato-mandibularis

Art.qpt:

Art. quadrato-pterygoidea

Art.qqj:

Art. quadrato-quadratojugalis

Art.qso:

Art. quadrato-squamoso-otica

BH:

Basihyale

BHD:

Basihyoideum (mammals)

C.ling:

Corpus linguae

CAN:

Canine tooth (mammals)

Cart.ar:

Cartilago arytaenoidea (mammals)

Cart.cr:

Cartilago cricoidea (mammals)

Cart.thy:

Cartilago thyroidea (mammals)

CASC:

Subcutaneous cervical air sac of the cervico-cephalic air sac system

Cav.lrx:

Cavum laryngis, laryngeal chamber

Cav.nas:

Cavum nasale

Cav.or:

Cavum oris, oral or mouth cavity

Cav.sbl:

Cavum sublinguale

Cav.syn:

Cavitas synovialis fasciae vaginalis

Cav.tymp:

Cavum tympanicum

CB:

Ceratobranchiale

Cer:

Cera, cere

Cerb:

Cerebrum

Cerbl:

Cerebellum

CH:

Choana

CHD:

Ceratohyoideum (mammals)

CL:

Clavicula, Furcula

Cond.mq:

Condylus mandibularis quadrati

Cond.occ:

Condylus occipitalis

Condd.occ:

Condyli occipitales (mammals)

Cot.qm:

Cotyla quadratica mandibulae

CR:

Cricoideum

CRd:

Cricoideum dorsale

CRv:

Cricoideum ventrale

SK:

Skull, braincase, Cranium

Cutl:

Cuticula cornificata linguae, the lingual nail

EB:

Epibranchial

EH:

Epihyoideum (mammals)

em:

Epimysium (of M. branchiomandibularis)

EPGL:

Epiglottis (mammals)

Fac.art.ar:

Facies articularis intra-arytenoidea

Fac.art.bc:

Facies articularis basihyalis ceratobranchialis

Fac.art.buh:

Facies articularis basihyo-urohyalis

Fac.art.cb:

Facies articularis ceratobranchialis basihyalis

Fac.art.mq:

Facies articularis mandibularis quadrati

Fac.art.par:

Facies articularis processus arytenoidei

Fac.art.phe:

Facies articularis pharyngobranchialis epibranchialis

Fac.art.qm:

Facies articularis quadratica mandibulae

F.cerv:

Fascia cervicalis

F.sbl:

Fascia sublingualis

F.vag:

Fascia vaginalis hyoidei, hyoid sheath

F.vag.pv:

Fascia vaginalis hyoidei parietalis et visceralis

F.vagp:

Fascia vaginalis hyoidei parietalis

F.vagv:

Fascia vaginalis hyoidei visceralis

FM:

Foramen magnum

FR:

Filing ridges on internal surface of projecting upper bill tip in parrots and some cockatoos

GL:

Glottis

Gl.ling:

Glandula lingualis; Gll. linguales rostrales (McLelland 1993)

Gl.md:

Glandula mandibularis; Gll. mandibulares caudales (McLelland 1993)

Gl.mx:

Glandula maxillaris

Gl.pregl:

Glandula preglottalis; Glandulae linguales caudales (McLelland 1993)

Gl.phrx:

Glandula pharyngealis; Gll. sphenopterygoideae (Zweers 1982a, b)

Gl.sbl:

Glandula sublingualis; Gll. mandibulares rostrales (McLelland 1993)

Gl.pl:

Glandula palatina

HP:

Hard, or secondary, palate (mammals)

IM.cnstr.crar:

Insertion of M. constrictor glottidis cricoarytenoideus

IM.cnstr.iarr:

Insertion of M. constrictor glottidis interarytenoideus rostralis

IM.cnstr.iars:

Insertion of M. constrictor glottidis interarytenoideus superficialis

IM.dlgl:

Insertion of M. dilator glottidis

INC:

Incisor tooth (mammals)

INGL:

Ingluvies, crop

INT:

Integument (skin)

J:

Os jugale

Lab.gl:

Labium glottidis

Lab.or:

Labium oralis (mammals)

Lb.pl:

Lobus palatinus

Lig.iph:

Ligamentum interparahyale

Lig.crar:

Ligamentum crico-arytenoideum

Lig.nc:

Ligamentum nodulo-ceratobranchiale

Lig.po:

Ligamentum postorbitale

Lphrx:

Laryngopharynx (mammals)

LP:

lips, Labia oris (mammals)

LX:

Larynx

M.ame:

M. adductor mandibulae externus

M.amec:

M. adductor mandibulae externus caudalis

M.amerl:

M. adductor mandibulae externus rostralis lateralis

M.amert:

M. adductor mandibulae externus rostralis temporalis

M.amev:

M. adductor mandibular externus ventralis

M.bm:

M. branchiomandibularis

M.bmr:

M. branchiomandibularis rostralis

M.bmc:

M. branchiomandibularis caudalis

M.cg:

M. ceratoglossus

M.cgl:

M. ceratoglossus lateralis

M.ch:

M. ceratohyoideus

M.cnstr:

M. constrictor glottidis

M.cnstr.crar:

M. constrictor glottidis cricoarytenoideus

M.cnstr.iarc:

M. constrictor glottidis interarytenoideus caudalis

M.cnstr.iarr:

M. constrictor glottidis interarytenoideus rostralis

M.cnstr.iars:

M. constrictor glottidis interarytenoideus superficialis

M.cnstr.icr:

M. constrictor glottidis intercricoideus

M.crh:

M. cricohyoideus

M.crhd:

M. cricohyoideus dorsalis

M.crhdi:

M. cricohyoideus dorsalis intermedius

M.crhdp:

M. cricohyoideus dorsalis profundus

M.crhds:

M. cricohyoideus dorsalis superficialis

M.crhl:

M. cricohyoideus lateralis

M.crhm:

M. cricohyoideus medialis

M.crhv:

M. cricohyoideus ventralis

M.crpp:

M. cricopapillaris profundus

M.crps:

M. cricopapillaris superficialis

M.dlgl:

M. dilator glottidis

M.dt:

M. dermotemporalis

M.em:

M. ethmomandibularis

M.dm:

M. depressor mandibulae

M.ggl:

M. genioglossus

M.ho:

M. hyoglossus obliquus

M.hol:

M. hyoglossus obliquus lateralis

M.hom:

M. hyoglossus obliquus medialis

M.hgr:

M. hyoglossus rostralis

M.mgl:

M. mesoglossus

M.mhr:

M. mylohyoideus rostralis

M.mhc:

M. mylohyoideus caudalis

M.pq:

M. protractor quadrati

M.pss:

M. pseudotemporalis superficialis

M.pt:

M. pterygoideus

M.ptl:

M. pterygoideus lateralis

M.pvl:

M. pterygoideus ventralis lateralis

M.retr.pl:

M. retractor pterygopalatini

M.sgl:

M. supraglossus

M.sh:

M. serpihyoideus

M.st:

M. stylohyoideus

M.sth:

M. sternohyoideus (mammals)

M.th:

M. tracheohyoideus

M.thc:

M. tracheohyoideus caudalis

M.thr:

M. tracheohyoideus rostralis

M.tl:

M. tracheolateralis

M.tll:

M. tracheolateralis lateralis

M.tlm:

M. tracheolateralis medialis

M.tlu:

M. tracheolateralis urohyalis

MD:

Os mandibulare, mandible

Med.obl:

Medulla oblongata

Med.sp:

Medulla spinalis

Mem.pl:

Membrana connectiva palatina (palatine joint membrane between the corneous and soft parts of the palate)

MH:

Mesohyoideum

Mm.lrx:

Laryngeal muscles

Mm.ling:

Lingual muscles

Mns.lrx:

Mons laryngealis

MOL:

Molar tooth (mammals)

N:

Naris

NCASC:

Passageway between naris and cervical air sac CASC

ND:

Nodulus (sesamoid bone on the urohyal)

Neck:

Neck (vertebral column and neck musculature)

Nphrx:

Nasopharynx (mammals)

OC:

Optic chiasma

OE:

Esophagus

OM.cnstr.crar:

Origin of M. constrictor glottidis cricoarytenoideus

OM.cnstr.iarc:

Origin of M. constrictor glottidis interarytenoideus caudalis

OM.cnstr.iarr:

Origin of M. constrictor glottidis interarytenoideus rostralis

OM.cnstr.icr:

Origin of M. constrictor glottidis intercricoideus

OM.dlgl:

Origin of M. dilator glottidis

Ophrx:

Oropharynx (mammals)

Papp.ch:

Papillae choanales

Papp.gl:

Papillae glottidiales

Papp.lrx:

Papillae laryngeales; ventral pharyngeal scrapers (Zweers and Berkhoudt 1987)

Papp.ling:

Papillae linguales

Papp.phrx:

Papillae pharyngeales

Papp.pl:

Papillae palatinae

PASP:

Parapatagial air sac of the pulmonary air sac system

PB:

Pharyngobranchiale

PC:

Procricoideum

PG:

Paraglossum

PIT:

Pituitary gland

PL:

Os palatinum

Pl.corn:

Palatum corneum

Plut.ch:

Pluteum choanae, lateral choanal shelf

PM:

Premolar tooth (mammals)

Proc.ar:

Processus arytenoideus

Proc.lat:

Processus lateralis quadrati

Proc.mq:

Processus mandibularis quadrati

Proc.mst:

Processus mastoideus (mammals)

Proc.orb:

Processus orbitalis quadrati

Proc.ot:

Processus oticus quadrati

Proc.ph:

Processus parahyalis

Proc.po:

Processus postorbitalis

Proc.rtr:

Processus retroarticularis mandibulae

Proc. uh:

Processus urohyalis

Proc.zyg:

Processus zygomaticus

PT:

Os pterygoideum

Q:

Os quadratum

R.mx:

Rostrum maxillare, maxilla, upper beak

R.sph:

Rostrum sphenoidale

Ram.md:

Ramus mandibularis

Rh.md:

Rhamphotheca mandibularis

Rh.mx:

Rhamphotheca maxillaris

Rim.inf:

Rima infundibuli, entrance to the Eustachian tubes

Sin.f:

Sinus frontalis (mammals)

Sin.sph:

Sinus sphenoidalis (mammals)

SPL:

Soft palate (mammals)

STH:

Stylohyoideum (mammals)

SX:

Syrinx

T:

Tongue (mammals)

T.md:

Tomium mandibulare, cutting edge of the mandibular rhamphotheca

TB:

Tympanic bulla (mammals)

TMH:

Tympanohyoideum (mammals)

Tor.pl:

Torus palatinus

TR:

Trachea

TRh:

Tracheal half rings

TYH:

Thyrohyoideum (mammals)

TS:

Transverse step of the corneous palate (Gradus transversus palati cornei)

VERT:

Vertebral column

VF:

Vocal fold, Plica vocalis (mammals)

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Homberger, D.G. (2017). The Avian Lingual and Laryngeal Apparatus Within the Context of the Head and Jaw Apparatus, with Comparisons to the Mammalian Condition: Functional Morphology and Biomechanics of Evaporative Cooling, Feeding, Drinking, and Vocalization. In: Maina, J. (eds) The Biology of the Avian Respiratory System. Springer, Cham. https://doi.org/10.1007/978-3-319-44153-5_2

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