Osteology of the feeding apparatus of Magnificent Frigatebird Fregata magnificens and Brown Booby Sula leucogaster (Aves: Suliformes)

Authors

  • Caio José Carlos Universidade Federal do Rio Grande do Sul Departamento de Zoologia Laboratório de Sistemática e Ecologia de Aves e Mamíferos Marinhos http://orcid.org/0000-0001-9071-1444
  • Jéssica Guimarães Alvarenga Universidade Federal do Rio Grande do Sul Departamento de Zoologia Laboratório de Sistemática e Ecologia de Aves e Mamíferos Marinhos
  • Mariana Scain Mazzochi Universidade Federal do Rio Grande do Sul Departamento de Zoologia Laboratório de Sistemática e Ecologia de Aves e Mamíferos Marinhos

DOI:

https://doi.org/10.11606/0031-1049.2017.57.20

Keywords:

Functional anatomy, Jaw apparatus, Mandible musculature, Seabirds, Syncranium

Abstract

In this paper, we describe the skulls of Magnificent Frigatebird Fregata magnificens (Fregatidae) and Brown Booby (Sulidae) Sula leucogaster, with focus on the structures associated with the Musculi mandibulae. We discuss the results in the context of the feeding biology of the two species, which feed mainly on flying fish and squids. Frigatebirds capture prey from just above, or just below, the water surface in flight. The hook-shaped Apex maxillae in F. magnificens can be viewed as an adaptation for grasping prey from near the water surface. Boobies catch prey by plunging; thus, the dorsoventrally flattened skull and conical bill of S. leucogaster may reduce water resistance when it dives, or swims underwater. The bill is long in both species, such that it is on average 70% of the whole skull length in F. magnificens and 60% in S. leucogaster. Consequently, the Mm. mandibulae in the two species are more posteriorly positioned relative to the Apex rostri. This results in low mechanical advantage for the mandible opening-closing lever, indicating adaptations for a fast, rather than a strong, bite. Fast-moving mandibles would be advantageous for ‘mandibulating’ prey while swallowing. The Fossa musculorum temporalium and the Palatum osseum in both species provide a broad area for origins of the Musculus adductor mandibulae externus (all parts) and the Musculus pterygoideus. The Processus orbitalis quadrati is longer and thicker in F. magnificens than in S. leucogaster, and so is the Musculus pseudotemporalis profundus. We suggest that Mm. adductores mandibulae are relatively well developed in the two species; therefore, their mandibulae are still probably capable of a powerful adduction. In both species there is a mechanisms that contribute to protect the jaws from disarticulation and damage. Such mechanism involves the incorporation of a ‘flange-like’ Crista intercotylare on the Margo medialis cotylae medialis fossae articularis quadratica that grips the Condylus medialis quadrati. In S. leucogaster, the retractor-stop ‘notch’ formed by Ossa lacrimale et nasale also serves to protect the jaws against sudden external forces when birds are diving or swimming underwater for prey. A more detailed hypothesis for the jaw movements and strength in F. magnificens and in S. leucogaster and their relation with feeding habits should necessarily incorporate data on the jaw and anterior neck musculatures.

Downloads

Download data is not yet available.

Author Biographies

  • Caio José Carlos, Universidade Federal do Rio Grande do Sul Departamento de Zoologia Laboratório de Sistemática e Ecologia de Aves e Mamíferos Marinhos

    Avenida Bento Gonçalves, 9.500, Agronomia
    CEP 91501-970, Porto Alegre, RS, Brasil

  • Jéssica Guimarães Alvarenga, Universidade Federal do Rio Grande do Sul Departamento de Zoologia Laboratório de Sistemática e Ecologia de Aves e Mamíferos Marinhos

    Avenida Bento Gonçalves, 9.500, Agronomia
    CEP 91501-970, Porto Alegre, RS, Brasil

  • Mariana Scain Mazzochi, Universidade Federal do Rio Grande do Sul Departamento de Zoologia Laboratório de Sistemática e Ecologia de Aves e Mamíferos Marinhos

    Avenida Bento Gonçalves, 9.500, Agronomia
    CEP 91501-970, Porto Alegre, RS, Brasil

References

Ashmole, N.P. 1968. Body size, prey size and ecological segregation in five sympatric tropical terns. Systematic Zoology, 17:292‑304.

Baumel, J.J. & Witmer, L.M. 1993. Osteologia. In: Baumel, J.J.; King, A.S.; Breazile, J.E.; Evans, H.E. & Vanden Berge, J.C. (Eds.). Handbook of avian anatomy: Nomina anatomica avium. 2.ed. Cambridge, MA, Nuttall Ornithological Club. p. 45‑133.

Beddard, F.E. 1897. Notes upon the anatomy of Phaethon. Proceedings of the Zoological Society of London, 1897:288‑295.

Bock, W.J. 1960. Secondary articulation of the avian mandible. Auk, 77:19‑55.

Bock, W.J. 1964. Kinetics of the avian skull. Journal of Morphology, 114:1‑42.

Branco, J.O.; Fracasso, H.A.A.; Machado, I.F.; Bovendorp, M. & Verani, J.R. 2005. Dieta de Sula leucogaster Boddaert (Sulidae, Aves), nas Ilhas Moleques do Sul, Florianópolis, Santa Catarina, Brasil. Revista Brasileira de Zoologia, 22:1044‑1049.

Branco, J.O.; Fracasso, H.A.A.; Machado, I.F.; Evangelista, C.L. & Hillesheim, J.C. 2007. Alimentação natural de Fregata magnificens (Fregatidae, Aves) nas Ilhas Moleques do Sul, Santa Catarina, Brasil. Revista Brasileira de Ornitologia, 15:73‑79.

Burger, A.E. 1978. Functional anatomy of the feeding apparatus of four South African cormorants. Zoologica Africana, 13:81‑102.

Burton, P.J.K. 1974. Feeding and the feeding apparatus in waders: a study of the anatomy and adaptations in the Charadrii. London, British Museum (Natural History).

Burton, P.J.K. 1984. Anatomy and evolution of the feeding apparatus in the avian orders Coraciiformes and Piciformes. Bulletin of the British Museum (Natural History), 47:331‑443.

Calixto-Albarrán, I. & Osorno, J.‑L. 2000. The diet of the Magnificent Frigatebird during chick rearing. Condor, 102:569‑576.

Carlos, C.J. 2015. Relações filogenéticas do “Clado das Aves Aquáticas”, com ênfase nas “Aves Totipalmadas” (Aves: Natatores aut Aequornithes). Ph.D. Thesis. Universidade Federal do Rio Grande do Sul, Porto Alegre.

Chesser, R.T.; Banks, R.C.; Barker, F.K.; Cícero, C.; Dunn, J.L.; Kratter, A.W.; Lovette, I.J.; Rasmussen, P.C.; Remsen Jr., J.V.; Rising, J.D.; Stoz, D.F. & Winker, K. 2010. Fifty-First Supplement to the American Ornithologists’ Union Check-List of North American Birds. Auk, 127:726‑744.

Clapp, R.B.; Banks, R.C.; Morgan-Jacobs, D. & Hoffman, W.A. 1982. Marine birds of the southeastern United States and Gulf of Mexico. Part I. Gaviiformes through Pelecaniformes. Washington, D.C., U.S. Fish and Wildlife Service, Office of Biological Services.

Cracraft, J. 1968. The lacrimal-ectethmoid bone complex in birds: a single character analysis. The American Midland Naturalist, 80:316‑359.

del Hoyo, J.; Elliot, A. & Sargatal, J. (Eds.). 1992. Handbook of the Birds of the World. Lynx Edicions, Barcelona, vol. 1.

Diamond, A.W. & Schreiber, E.A. 2002. Magnificent Frigatebird (Fregata magnificens). In: Poole, A. & Gill, F. (Eds.). The birds of North America. Philadelphia Academy of Natural Sciences; American Ornithologists’ Union, (601):1‑24.

Donatelli, R.J. 1996. The jaw apparatus of the neotropical and of the afrotropical woodpeckers (Aves: Piciformes). Arquivos de Zoologia, 33:1‑70.

Donatelli, R.J.; Höfling, E. & Catalano, A.L. 2014. Relationship between jaw apparatus, feeding habit, and food source in oriental woodpeckers. Zoological Science, 31:223‑227.

Hackett, S.J.; Kimball, R.T.; Reddy, S.; Bowie, R.C.K.; Braun, E.L.; Braun, M.J.; Chojnowki, J.L.; Cox, W.A.; Han, K.L.; Harshman, J.; Huddleston, C.J.; Marks, B.D.; Miglia, K.J.; Moore, W.S.; Sheldon, F.H.; Steadman, D.W.; Witt, C.C. & Yuri, T. 2008. A phylogenomic study of birds reveals their evolutionary history. Science, 320:1763‑1768.

Jarvis, E.D.; Mirarab, S.; Aberer, A.J.; Li, B.; Houde, P.; Li, C.; Ho, S.Y.W.; Faircloth, B.C.; Nabholz, B.; Howard, J.T.; Suh, A.; Weber, C.C.; Fonseca, R.R.; Li, J.; Zhang, F.; Li, H.; Zhou, L.; Narula, N.; Liu, L.; Ganapathy, G.; Boussau, B.; Bayzid, S.; Zavidovych, V.; Subramanian, S.; Gabaldón, T.; Capella-Gutiérrez, S.; Huerta-Cepas, J.; Rekepalli, B.; Munch, K.; Schierup, M.; Lindow, B.; Warren, W.C.; Ray, D.; Green, R.E.; Bruford, M.W.; Zhan, X.; Dixon, A.; Li, S.; Li, N.; Huang, Y.; Derryberry, E.P.; Bertelsen, M.F.; Sheldon, F.H.; Brumfield, R.T.; Mello, C.V.; Lovell, P.V.; Wirthlin, M.; Schneider, M.P.C.; Prosdocimi, F.; Samaniego, J.A.; Velazquez, A.M.V.; Alfaro-Núñez, A.; Campos, P.F.; Petersen, B.; Sicheritz-Ponten, T.; Pas, A.; Bailey, T.; Scofield, P.; Bunce, M.; Lambert, D.M.; Zhou, Q.; Perelman, P.; Driskell, A.C.; Shapiro, B.; Xiong, Z.; Zeng, Y.; Liu, S.; Li, Z.; Liu, B.; Wu, K.; Xiao, J.; Yinqi, X.; Zheng, Q.; Zhang, Y.; Yang, H.; Wang, J.; Smeds, L.; Rheindt, F.E.; Braun, M.; Fjeldsa, J.; Orlando, L.; Barker, F.C.; Jønsson, K.A.; Johnson, W.; Koepfli, K.; O’Brien, S.; Haussler, D.; Ryder, O.A.; Rahbek, C.; Willerslev, E.; Graves, G.R.; Glenn, T.C.; McCormack, J.; Burt, D.; Ellegren, H.; Alström, P.; Edwards, S.V.; Stamatakis, A.; Mindell, D.P.; Cracraft, J.; Braun, E.L.; Warnow, T.; Jun, W.; Gilbert, M.T.P. & Zhang, G. 2014. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science, 346:1320‑1331.

Livezey, B.C. & Zusi, R.L. 2006a. Variation in the os palatinum and its structural relation to the Palatum osseum of birds (Aves). Annals of Carnegie Museum, 75:137‑180.

Livezey, B.C. & Zusi, R.L. 2006b. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy: I. – Methods and characters. Bulletin of Carnegie Museum of Natural History, 37:1‑556.

Livezey, B.C. & Zusi, R.L. 2007. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and discussion. Zoological Journal of the Linnean Society, 149:1‑95.

Machovsky Capuska, G.E.; Dwyer, S.L.; Alley, M.R.; Stockin, K.A. & Raubenheimer, D. 2011. Evidence for fatal collisions and kleptoparasitism while plunge-diving in Gannets. Ibis, 153:631‑635.

Matsui, H.; Hunt, G.R.; Oberhofer, K.; Ogihara, N.; McGowan, K.J.; Mithraratne, K.; Yamasaki, T.; Gray, R.D. & Izawa, E.‑I. 2016. Adaptive bill morphology for enhanced tool manipulation in New Caledonian crows. Scientific Reports, 6:22776.

Mayr, G. 2010. Metaves, Mirandornithes, Strisores and other novelties – A critical review of the higher-level phylogeny of Neornithine birds. Journal of Zoological Systematics and Evolutionary Research, 49:58‑76.

Nelson, J.B. 1976. The breeding biology of frigatebirds: a comparative review. Living Bird, 14:113‑155.

Nelson, J.B. 1978. The Sulidae: gannets and boobies. Oxford, UK Oxford University Press.

Owre, O.T. 1967. Adaptations for locomotion and feeding in the anhinga and the double-crested cormorants. Ornithological Monographs, 6:1‑138.

Posso, S.R. & Donatelli, R.J. 2005. Skull and mandible formation in the cuckoo (Aves, Cuculidae): Contributions to the nomenclature in avian osteology and systematics. European Journal of Morphology, 42:163‑172.

Previatto, D.M. & Posso, S.R. 2015a. Cranial osteology of Cyclarhis gujanensis (Aves: Vireonidae). Papéis Avulsos de Zoologia, 55:255‑260.

Previatto, D.M. & Posso, S.R. 2015b. Jaw musculature of Cyclarhis gujanensis (Aves: Vireonidae). Brazilian Journal of Biology, 75:655‑661.

Pycraft, W.P. 1898. Contribution to the osteology of birds. Part I. Steganopodes. Proceedings of the Zoological Society of London, 1898:82‑101.

Schreiber, E.A. & Burguer, J. 2001. Seabirds in the marine environment. In: Schreiber, E.A. & Burguer, J. (Eds.). Biology of marine birds. Boca Raton, CRS Press. p. 1‑15.

Schreiber, E.A. & Norton, R.L. 2002. Brown Booby (Sula leucogaster). In: Poole, A. & Gill, F. (Eds.). The birds of North America. Philadelphia, Academy of Natural Sciences; American Ornithologists’ Union, (649):1‑28.

Schreiber, R.W. & Clapp, R.B. 1987. Pelecaniform feeding ecology. In: Croxall, J.P. (Ed.). Seabirds: feeding ecology and role in marine ecosystems. Cambridge, UK, Cambridge University Press. p. 173‑178.

Shufeldt, R.D. 1888. Observations on the osteology of the orders Tubinares and Steganopodes. Proceedings of the United States National Museum, 11:253‑315.

Shufeldt, R.D. 1902. The osteology of the Steganopodes. Memoirs of the Carnegie Museum, 1:109‑223.

Silva, A.G.; Bolzani, G.J.F.; Donatelli, R.J. & Guzzi, A. 2012. Osteologia craniana de Micrastur semitorquatus Vieillot, 1817 (Falconiformes: Falconidae). Comunicata Scientiae, 3:64‑71.

Smith, N.D. 2010. Phylogenetic analysis of Pelecaniformes (Aves) based on osteological data: Implications for waterbird phylogeny and fossil calibration studies. Plos One, 5:e13354.

Vanden Berge, J.C. & Zweers, G.A. 1993. Myologia. In: Baumel, J.J.; King, A.S.; Breazile, J.E.; Evans, H.E. & Vanden Berge, J.C. (Eds.). Handbook of avian anatomy: Nomina anatomica avium. 2.ed. Cambridge, MA, Nuttall Ornithological Club. p. 189‑247.

Zusi, R.L. 1962. Structural adaptations of the head and neck in the black skimmer, Rynchops nigra, L. Nuttall Ornithological Club, Cambridge, MA.

Zusi, R.L. 1967. The role of the depressor mandibulae muscle in kinesis of the avian skull. Proceedings of the United States National Museum, 123:1‑28.

Zusi, R.L. & Livezey, B.L. 2000. Homology and phylogenetic implications of some enigmatic cranial features in galliform and anseriform birds. Annals of Carnegie Museum, 69:157‑193.

Downloads

Published

2017-06-13

Issue

Section

Original Article

How to Cite

Carlos, C. J., Alvarenga, J. G., & Mazzochi, M. S. (2017). Osteology of the feeding apparatus of Magnificent Frigatebird Fregata magnificens and Brown Booby Sula leucogaster (Aves: Suliformes). Papéis Avulsos De Zoologia, 57(20), 265-274. https://doi.org/10.11606/0031-1049.2017.57.20