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Functional Morphology of the Enlarged Pharynx and Hyoid Bone of the

Hideki ENDO1, 2, 3, 4）＊, Takeshi YAMASAKI4）, Kent MORI1, 2）, Kohei KUDO1, 3） and Daisuke KOYABU1）

1） The University Museum, The University of , Tokyo 113-0033, Japan 2） Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo 113-0033, Japan 3） Department of Global Agricultural Sciences, Graduate School of Agriculture and Agricultural Life Sciences, The University of Tokyo, Tokyo 113-0033, Japan 4） Yamashina Institute for , Abiko, Chiba 270-1145, Japan ［Received 5 May 2013; accepted 11 November 2013］

ABSTRACT The cavity of the pharynx and hyoid bone of the shoebill (Balaeniceps rex) were examined by using the three dimensional computed tomography image analysis. The pharynx and the cranial part of the esophagus were extraordinarily bilaterally enlarged. The unfixed flexible hyoid bone and degenerated tongue were discerned. We suggest that these morphological characteristics functionally enable the to receive the large prey item peculiar to the feeding behavior of the shoebill. The structure of the pharynx region may totally act as a flexible pouch to pass the large food to the alimentary tract. The bilateral asymmetry was also confirmed in the hyoid bone, cavities of the pharynx and cranial esophagus. We think that these asymmetrical forms may also contribute to the deglutition of large prey fish in the shoebill. Key words: asymmetry, deglutition, hyoid bone, pharynx, shoebill － Jpn. J. Zoo. Wildl. Med. 19（1）：21-25，2014

prey on large fish [8] has attracted the ecological researchers INTRODUCTION dealing with the feeding behavior, the morphological The shoebill (Balaeniceps rex) has been considered as one adaptation to deglutition of large food item is expected to of the strangest and rarest in the world. The species has functionally examine in the oral and pharyngeal cavities in been traditionally classified within Cicconiiformes together this species. Here, in this study, we observed the functional with and [1]. However, its phylogenetic morphological specialization in the pharynx region by the position has remained unclear, since the intermediate feature three-dimensional (3D) Computed Tomography (CT) image of -like and -like forms was confirmed in the analysis. shoebill [2-4]. Recently the morphological characteristics [4, MATERIALS AND METHODS 5] and the molecular phylogenetic data [6] have pointed out that the shoebill is closely related to the (Pelicanidae A male shoebill (Balaeniceps rex) used in this study has been or Pelecanus), whereas the biochemical traits of the biliary kept in Chiba Zoological Park (Chiba, Japan) and was donated bile acid indicated the genetic affinities between the shoebill to The University Museum, The University of Tokyo as a and [7]. However, morphological characteristics that specimen. The individual has been maintained since 1997 and functionally support the behavior peculiar to this species have was dead in 19 December 2009. After pathological checks, a disturbed us to reveal the evolutionary history of the shoebill. carcass was used for the analysis. The head and neck regions Since the feeding behavior in which the species ambush and were serially sectioned by CT (Asteion PREMIUM 4 EDITION, Toshiba Medical Systems, Tokyo, Japan) from the rostral to the caudal planes in parallel at 1mm thickness without * Corresponding author： gap. The two statuses of the closing and maximum opening Hideki ENDO (E-mail: [email protected]) mandible were simulated and scanned. We also applied Voxel

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Fig.1 Ventral aspect of the caudal part of the head. The Fig. 2 Dorsal aspect of the caudal part of the head. The hyoid bone (arrows) inclines to the right side and supports cranial region of the neck inclines to the right side (arrows). the cranial region of the trachea (T). The hyoid bone (arrows) is surrounded and covered with M. intermandibularis (asterisk) and M. epibranchialis mandibularis (EM). The esophagus (E) is bilaterally widened in its cranial part. I, M. interceratobranchialis; M, mandible.

Transmission (Volume Rendering) techniques to visualize the intact cervical and thoracic vertebrae, using a 3D image analyzing system (AZE Virtual Place, AZE Corporation, Tokyo, Japan). In addition to the CT observations, the head and neck regions were dissected. The morphological relationships between the hyoid bone and mandible were macroscopically observed. The anatomical nomenclature was fundamentally based on the Atlas of the [9]. The skin and skeletal specimens were prepared and stored in The University Museum, The University of Tokyo.

RESULTS

The hyoid bone was surrounded and covered with M. intermandibularis (Fig. 1). The hyoid bone was supported from rostral area by the M. intermandibularis and from rostro- lateral direction by M. epibranchialis mandibularis. This region around the hyoid bone obviously indicated the bilateral Fig.3 3D reconstructed images of the head from left (A) asymmetry in this individual. The basihyoideum and the rostral and right (B) lateral, and ventral (C) aspects. The soft parts have been partially removed from the images. The statuses of part of the hyoid bone were situated in the right side from the opening mandible (A, B) and closing mandible (C) are shown. sagittal line. The hyoid bone did not represent the isosceles The osteologically unfixed hyoid bone (large arrows) inclines triangle but triangle shape elongated to the right lateral side. to the right and ventral directions. The row of the cartilages of The caudal part of the hyoid bone did not reach the occipital the trachea is confirmed (small arrows).

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area of the skull. The neck also inclined to right side in the DISCUSSION most cranial area (Fig. 2). The rostral part of the trachea also ran in the right side with the rostral part of the hyoid bone. Since the aves without teeth cannot crush food during the The most cranial part of the esophagus was bilaterally widened mastication, the other morphological or functional adaptation from ventral aspect (Fig. 2). is needed to the feeding action. For example, the large size of The 3D reconstructed images after partially rejecting soft the food item requires the ballistic food transport in toucans parts are shown from lateral and ventral aspects (Fig. 3). The and hornbills as a functional adaptation of deglutition [10, 11]. dorso-ventrally enlarged could be largely open. The The shoebill ambushes and preys on large fish such as marbled caudal part of the asymmetrical hyoid bone was observed or Senegal birch of 15-50 cm in body length, after it in caudo-medial space of the mandible. The hyoid bone did remained statue-like still for long periods as mimicry [8]. As not possess the direct attachment area to the skull and was the size of a single food item is larger in this feeding behavior, physically supported only by the soft parts. The lateral views the mechanism of the deglutition mechanism should be show that the distance between the ventral margin of the functional-morphologically adapted to the large-sized prey. In mandible and hyoid bone body was much larger in right side this study, the enlargement of the cavities of the pharynx and than in the left side. The images also showed that the hyoid cranial esophagus could be confirmed from 3D reconstructed bone inclines to the right and ventral directions. images. The large beak and bilaterally enlarged pharynx and The 3D sectioning techniques reveals the morphological esophagus enable the species to pass large prey items to the relationships between the hyoid bone and pharynx (Figs 4 alimentary tract. From the CT images, we demonstrated that and 5). The cavity of the pharynx was ventrally supported by the hyoid bone fixed the shape of the enlarged pharynx in both the hyoid bone and extraordinarily bilaterally enlarged (Fig. statuses of the closing and opening mandible. 4). The bilateral space of the cavity of the pharynx formed the The degenerated tongue indicated by Mitchell [12] may Recessus piriformis. The right side of the cavity of the pharynx also contribute to the enlarged space in caudal area of the and esophagus was not only rostrally but also ventrally oral cavity in this species. As the shoebill has been functional- enlarged (Figs 3-5) The 3D CT axial sections demonstrated morphologically specialized during the evolutionary history, that the hyoid bone pulled the oral, pharyngeal and cranial we suggest that the tongue had been secondarily degenerated esophagus cavities rostro-dorsally in right side, and caudo- in this species. The lack of the direct attachment between the ventrally in the left side (Figs. 4 and 5). The most cranial region hyoid bone and the skull is consistent with the degeneration of of the trachea and the Aditus laryngis inclined to the right side the tongue. The evolutionarily undeveloped tongue and unfixed to accompany the asymmetrical hyoid bone. The tongue was so hyoid bone suggest that the action of the tongue may not be highly degenerated in rostral pharyngeal cavity. functionally important in this species. We can conclude that The shape similarities or differences of the oral and the structure of the pharynx region may totally act as a flexible pharyngeal cavities were revealed between the closing and pouch to receive and pass the large prey in the shoebill. opening statuses of mandible. Since the floor of the oral cavity As only one material could be examined in this study, the ventrally moved, the volume of the rostral part of the oral degree of the asymmetry of the hyoid bone will be needed to cavity obviously changed between the two statuses (Figs. 4A reexamine in other cases. Since the trachea and esophagus and 5A). In contrast, as the hyoid bone physically supported generally run in the right lateral side of the neck in large- the ventral floor of the caudal oral and pharyngeal cavities (Figs. sized birds, it may be reasonable that the most cranial part of 4B, 4C, 5B and 5C), the shape of the cavities did not change in the trachea and the Aditus laryngis incline to the right side in the caudal part from the Aditus larynges between the closing the shoebill. The numbers of carcasses and specimens should and opening statuses of the mandible. Although the bundles of be compared between the shoebill and the other species with M. pterygoideus were latero-ventrally pulled according to the similar feeding behavior. However, it will be difficult to dissect angle of the mandible, the hyoid bone fixed the shape of the the additional as well as related species, since few caudal oral and pharyngeal cavities (Fig. 4B and 5B). individuals of the rare species have been maintained. The asymmetrical hyoid bone, pharynx and trachea

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Fig. 4 Rostral aspect of the axial section of the 3D reconstructed image of the head. The soft parts have been partially removed from the images. The status of the closing mandible is seen. Rostral region has been cut and removed in the level of the most rostral point of the hyoid bone (A), the Aditus laryngis (B), and the caudal part of the orbit (C). A) The hyoid bone (arrows) inclines to right and ventral direction. The degenerated tongue cannot be discerned around the hyoid bone. M, mandible. B) The cavity of the pharynx and esophagus (E) are enlarged in left lateral and ventral direction. The trachea (T) and Aditus laryngis (arrow) are seen. P, the section of bundles of M. pterygoideus; B, eyeball. C) The caudal parts of the hyoid bone (arrows) are confirmed in medial space of the mandible. E, bilateral asymmetrical cavity of the cranial esophagus.

Fig. 5 Rostral aspect of the axial section of the 3D reconstructed image of the head. The soft parts have been partially removed from the images. The status of the opening mandible is seen. Rostral region has been cut and removed in the level of the most rostral point of the hyoid bone (A), the Aditus laryngis (B), and the caudal part of the orbit (C). A) The floor of the oral cavity (asterisk) surrounds the hyoid bone (arrows) inclining to right and ventral direction. The tongue cannot be found. M, mandible. B) The cavity of the pharynx and esophagus (E) are enlarged in left lateral and ventral direction. The trachea (T) and Aditus laryngis (arrow) are seen. P, the section of bundles of M. pterygoideus; B, eyeball. The hyoid bone fixes the shape of the ventral side of the pharyngeal cavity, although the M. pterygoideus bundles are latero-ventrally pulled in comparison with the closing status of the mandible (Fig. 4B). C) The caudal parts of the hyoid bone (arrows) are confirmed in medial space of the mandible. E, bilateral asymmetrical cavity of the cranial esophagus.

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provide the species with the space of food passage during Proc Royal Soc Lond Ser B 268: 1-6. the deglutition of the large food. The shoebill can obtain the 4. Livezey BC, Zusi RL 2007. Higher- phylogeny of modern birds (, Aves: Neornithes) based on comparative elongated space from right-rostro-ventral to left-caudo-dorsal anatomy. II. Analysis and discussion. Zool J Linn Soc 149: 1-95. direction between oral cavity and cranial esophagus because of 5. Mayr G 2003. The phylogenetic affinities of the shoebill this asymmetry (Figs. 4 and 5). We suggest that the space may (Balaeniceps rex). J Ornithol 144: 157-175. be much elongated and enlarged in the real shoebill than in the 6. Hackett SJ, Kimball RT, Reddy S, Bowie RC, Braun EL, Braun MJ, assumptive symmetrical status of the same . Chojnowski JL, Cox WA, Han K-L, Harshman J, Huddleston CJ, Marks BD, Miglia KL, Moore WS, Sheldon FH, Steadman DW, Witt ACKNOWLEDGEMENTS CC, Yuri T. 2008. A phylogenomic study of birds reveals their evolutionary history. Science 320: 1763-1768. This study was financially supported by the Grant-in-Aids 7. Hagey JR, Schteingart CD, Ton-Nu H-T, Hofmann, AF. 2002. A for Scientific Research nos. 24000015, 24370035, 25304005 novel primary bile acid in the shoebill stork and herons and its and 23658253 from the JSPS and the Ministry of Education, phylogenetic significance.J Lipid Res 43: 685-690. Science and Culture, Japan. 8. Hancock JA, Kushlan JA, Philip Karl, M. 1992. Storks, , and Spoonbills of the World. Academic Press, New York. REFERENCES 9. Yasuda, M. 2002. The Anatomical Atlas of Gallus. The University of Tokyo Press, Tokyo. (in Japanese). 1. Elliot A. 1992. Balaeniceptidae (shoebill). In Handbook of the 10. Baussart S, Korsoun L, Libourel P-A, Bels V. 2009. Ballistic food Birds of the World (del Hoyo J, Elliot A, Sargatal J. eds.), vol. 1. pp. transport in toucans. J Exp Zool 311A: 465-474. 466-471. Lynx, Barcelona. 11. Baussart S, Bels, V. 2011. Tropical hornbills (Aceros cassidix, 2. Cottam PA. 1957. The pelecaniform characters of the skeleton of Aceros undulatus, and Buceros hydrocorax) use ballistic transport the shoebill stork, Balaeniceps rex. Br Mus (Nat Hist) Bull (Zool to feed with their large . J Exp Zool 315: 72-83. Ser) 5: 49-72. 12. Mitchell PC 1913. Observation on the anatomy of the shoe-bill 3. Van Tuinen M, Butvill DB, Kirsch JAW, Hedges SB. 2001. (Balaeniceps rex) and allied birds. Proc Zool Soc Lond 1913: 644- Convergence and divergence in the of aquatic birds. 703.

原著 解剖学 ハシビロコウの拡張した咽頭および舌骨の機能形態学 遠藤秀紀 1, 2, 3, 4），山崎剛史 4），森 健人 1, 2），工藤光平 1, 3），小薮大輔 1） 1）東京大学総合研究博物館 〒 113-0033 東京都文京区本郷 7-3-1 2）東京大学大学院理学系研究科生物科学専攻 〒 113-0033 東京都文京区本郷 7-3-1 3）東京大学大学院農学生命科学研究科農学国際専攻 〒 113-8657 東京都文京区弥生 1-1-1 4）公益財団法人山階鳥類研究所 〒 270-1145 千葉県我孫子市高野山 115 ［2013 年 5 月 5 日受領，2013 年 11 月 11 日採択］

要 約 ハシビロコウ（Balaeniceps rex）の咽頭腔と舌骨を三次元 CT 画像解析により検討した。咽頭と頭側の食道は，左右両側へ著し く拡大していた。巨大な咽頭と頭側の食道，固定されていない柔軟な舌骨，退化した舌が観察された。これらはハシビロコウがそ の採餌生態に特徴的な大きな食魂を受け止めることを可能にしていると考えられた。ハシビロコウの咽頭腔領域の構造は，大きな 食塊を消化管へ通過させる柔軟な憩室として機能していることが示唆された。また，舌骨，口腔，咽頭腔，頭側の食道腔に左右非 対称性が観察された。この非対称性もハシビロコウが大きな魚体を嚥下することに寄与している可能性がある。 キーワード：嚥下，咽頭，舌骨，ハシビロコウ，非対称 －日本野生動物医学会誌 19（1）：21-25，2014

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