呂君昌

中國地質(zhì)科學院地質(zhì)研究所, 國土資源部地層與古生物重點實驗室, 北京 100037

寬頜遼西翼龍(翼龍目)的舌器以及其攝食行為的啟示

呂君昌

中國地質(zhì)科學院地質(zhì)研究所, 國土資源部地層與古生物重點實驗室, 北京 100037

在翼龍類不同的類群中其攝食行為是不同的, 從其牙齒形狀以及石化的胃容物來判斷, 其攝食行為包括食魚類、食昆蟲類、濾食水中小的水生生物、食螃蟹和蝸牛等帶殼的動物, 以及食水果類等。由于生存的需要, 它們占據(jù)不同的生態(tài)灶, 決定了其食物來源的不同。本文描述了寬頜遼西翼龍一件幾乎完整、保存完好的與下頜在一起的舌器化石標本, 并且它與現(xiàn)生蜥蜴類變色龍的舌器對比。它長的舌突與運用其舌的外翻來攝取食物的現(xiàn)生蜥蜴類-變色龍相類似, 從而暗示了遼西翼龍可能具有類似的、用舌獲取食物的行為, 加上其獨特的牙齒形態(tài), 進一步提出遼西翼龍是食昆蟲類而不是食魚的翼龍。

舌器; 遼西翼龍; 翼龍目; 中國

Pterosaurs, a group of Mesozoic flying reptiles, have varying feeding-behaviors, judging from their dentitions and fossilized stomach contents (Wellnhofer, 1991). At present, about 50 genera belonging to 12 families of pterosaurs have been discovered in China, and make up almost half the number of known pterosaurs in the world. More and more species will continue to be discovered with the further research. China has become the richest country with pterosaur fossils discovered in the world (Lü et al., 2013). During the last 10 years, more than 20 new species of pterosaurs have been found in north-east China and this rate of discovery shows little signs of slowing. Among them, there are two important discoveries: One is the discovery of Darwinopterus (Lü et al., 2010a; Lü, 2010a), an evolutionarily intermedi-ate form that bridges the gap between the two main groups of pterosaurs, and it provides strong evidence for an unusual type of ‘modular’ evolution. The other is the discovery of a female Darwinopterus with her egg preserved (Lü et al., 2011a), this resolved the gender identification problem in pterosaurs, and also the question of the significance of the cranial crest which confused scientists for more than a hundred years has been answered.

Although there are many beautifully preserved pterosaurs found from middle Jurassic and Early Cretaceous deposits (Lü et al., 2013), only several pterosaurs were reported with hyoids preserved, such as Liaoxipterus brachyognathus (Dong and Lü, 2005), Feilongus youngi (Wang et al., 2005), Darwinopterus robustodens (Xu et al., 2010; Lü et al., 2011b) and Kunpengopterus sinensis (Wang et al., 2010), however, the structures of hyoid apparatus were not described in detail, and much less their functions.

Compared with the other skeletal parts, even a partial hyoid apparatus of a pterosaur is rare. The holotype specimen of Liaoxipterus includes an almost completely preserved hyoid apparatus (Dong and Lü, 2005; Lü et al., 2008). Its long processus lingualis (processus entoglossus) is similar to that of the modern reptile Chameleon, which uses it for lingual feeding behavior. Thus, it is possible that Liaoxipterus practiced lingual feeding behavior, which would be expected if it was an insect-eating pterosaur.

The feeding behavior of pterosaurs was varied in different groups. Some pterosaurs are filter-feeding, such as Ctenochasma (Meyer, 1851), Gnathosaurus (Meyer, 1834), Huanhepterus (Dong, 1982) and Pterodaustro (Bonaparte, 1971; Chiappe et al., 2000; Codorniú and Chiappe, 2004), and used their numerous long, slender teeth to filter small aquatic organisms out of the water (Wellnhofer, 1991; Codorniú and Chiappe, 2004). The strong crushing teeth of dsungaripterids implies that fish is probably not the only food for them, and some shelly organisms such as mollusks, snails and crabs may have been part of their diets too (Young, 1973; Wellnhofer, 1991). Many pterosaurs were piscivorous, including Rhamphorhychus, Eudimophodon, and Pterodactylus, whose stomach contents are made up of the remains of fish (Wellnhofer, 1991). Some long beaked, toothless pterosaurs, such as Queztalcoatlus, may have used their slender beaks to probe for molluscs and arthropods in shallow water (Langston, 1981; Wellnhofer, 1991) or for carrion and small animals (Lawson, 1975; Witton and Naish, 2008). Insect-eating pterosaurs included Anurognathus ammoni (Wellnhofer, 1991).

Liaoxipterus (Fig. 1) was initially assigned to the Ctenochasmatidae, based on the lower jaw and the tooth number which is fewer than typical ctenochasmatid pterosaurs (Dong and Lü, 2005). However, further repairing the specimen shows that the tooth and the lower jaw end morphologies of Liaoxipterus are similar to those of Istiodactylus, thus it is reassigned to Istiodactylidae (Lü et al., 2006).

圖1　和舌器保存在一起的遼西翼龍的下頜骨(A)和下頜前部的放大(B)Fig. 1　The lower jaw of Liaoxipterus with a hyoid apparatus preserved (A) and close up of the anterior portion of the lower jaw (B)

The hyoid apparatus supports and moves the tongue and, to a lesser degree, the larynx (Romer, 1956). While the hyoid apparatus is informative with respect to the function of the tongue, and therefore in the inference of diet, none of these interpretations of pterosaur diet rely on the anatomy of the hyoid apparatus because, compared with the other skeletal parts, remains of the hyoid apparatus in pterosaurs are rare. Therefore, the almost complete hyoid apparatus of Liaoxipterus described here is particularly significant.

1　Description

The hyoid apparatus is derived from the hyoid arch and the two succeeding visceral arches (Romer, 1956). It lies in the floor of the mouth and pharynx and is associated with the musculature of that region. In derived lizards, it consists of an unpaired body, the corpus, tapering in a cranial direction into a narrower process, the processus lingualis (or processus entoglossus), which varies in length and is bound into the posterior part of the tongue, and three pairs of horns connected laterally in various ways with the corpus. The anterior pair is called the cornu hyale, the middle pair is the cornu branchiale I, and the posterior pair is the cornu branchiale II (Fürbringer, 1922; Colbert, 1945).

In modern reptiles, such as Anolis, the hyoid apparatus is entirely cartilaginous, except for the ceratobranchials I (Bels, 1990). Because the reptilian hyoid elements are relatively small, separate from major skeletal structures, and often unossified, their fossilforms, if are found, are consisted of a single pair of elements, which, by analogy with recent forms, are reasonably identified as first ceratobranchials (Romer,1956). Thus it is inferred that the two long, slender posteriorly extended branches of the hyoid apparatus in Liaoxipterus are ceratobranchials I and its ceratobranchials II are not preserved.

The hyoid apparatus of Liaoxipterus (Figs.1A, 2) is a Y-shaped group of small bones. The length of the corpus including the hypohyal or lingual process is 26.3 mm, and the diameter of the corpus is 1.27 mm. The whole length of the hyoid apparatus (from the tip of the lingual process to the distal end of the ceratobranchial I) is 107.85 mm. The divarication of the ceratobranchial I is 21o (Lü et al., 2008). The highly elongated lingual process of the hyoid apparatus in Liaoxipterus is similar to that of Chameleon, while the elongated ceratobranchial I is similar to that of Vipera (Fig. 2), however, it is difficult to know whether the elongated ceratobranchials have a same function or not. Because the the ceratobranchial II in Liaoxipterus is cartilaginous, and it is not preserved as fossil element, the shape of the hyoid apparatus is different from that of the chameleon (Fig.2D). The tongue is connected to the relatively long entoglossal process (Bels, 1990), the elongated lingual processes between these two taxa are similar, thus they may play the same function.

圖2　現(xiàn)生爬行動物及其他翼龍類的舌器與遼西翼龍的舌器比較Fig. 2　A comparison of hyoids in other pterosaurs and the living reptiles with that of LiaoxipterusA-喙頭目: 楔齒蜥屬; B-有鱗目: Lacerta; C-蜥蜴; D-變色龍; E-有鱗目: 蝰蛇; F-壯齒達爾文翼龍; G-玩具翼龍屬; H-遼西翼龍; A, B, E據(jù)Colbert, 1945; C, D據(jù)Kardong, 1998; 未按比例尺; 縮寫: AP-前突起; Bh-基舌骨; C-主體, 包括下舌骨或舌內(nèi); Ch-cornu hyale角舌骨和上舌骨; Cbl-第一角鰓骨; Cb2-第二角鰓骨; Lp-舌突A-Rhynchocephalia: Sphenodon; B-Squamata: Lacerta; C-a lizard without a projectile tongue; D-the chameleon (the hyoid apparatus includes an elongated lingual process (LP) along which the tongue slides during launch; E-Squamata, Vipera; F-Darwinopterus robustodens (drawn from Lü et al., 2011b); G-Ludodactylus (Drawn from Frey et al., 2003); H-Liaoxipterus; A, B, E are from Colbert, 1945; C, D are from Kardong, 1998; Not to scale; Key to abbreviations: AP-anterior process; Bh-basihyal; C-corpus, including the hypohyal or entoglossal; Ch-ceratohyal and epihyal, cornu hyale; Cbl-ceratobranchial I, cornu branchiale I; Cb2-ceratobranchial II, cornu branchiale II; Lp-lingual process

2　Comparison and Discussion

The hyoid apparatus of pterosaurs is rarely preserved, especially for the complete ones. This is perhaps due to the poor ossification and fragility of the hyoid apparatus in pterosaurs. At present, only few cases of pterosaur hyoid have been reported (Wellnhofer and Kellner, 1991; Frey et al., 2003; Wang et al., 2005; Lü et al., 2011b), but they were only briefly mentioned.

The first ceratobranchials of hyoid apparatus in Liaoxipterus are fused at their distal ends, and then extends anteriorly forming a long lingual process (Ap), which is similar to that of Ludodactylus (Fig.2G, 2H). They are different from those of Darwinopterus robustodens (Fig. 2F) and Tapejara wellnhoferi (Wellnhofer and Kellner, 1991), where the first ceratobranchials of hyoid apparatus are separated from each other.

The tooth morphologies of pterosaurs from western Liaoning and its surrounding areas indicate that various food-catching behaviors exist among them. The pterosaurs with long, pointed teeth, such as Feilongus (Wang et al., 2005), Boreaopterus (Lü and Ji, 2005), Zhenyuanopterus (Lü, 2010b), Liaoningopterus (Wang and Zhou, 2003), Gegepterus (Wang et al., 2007) and Fenghuangopterus (Lü et al., 2010b) are clearly fish-eating pterosaurs. The toothless forms, such as tapejarid pterosaurs, Sinopterus (Wang and Zhou, 2003; Li et al., 2003), Huaxiapterus (Lü and Yuan, 2005; Lü et al., 2006) may also be meat-eating pterosaurs or fruit-eating as proposed by Wellnhofer and Kellner (1991) for Tapejara, although there is no direct evidence to support it. Darwinopterus is regarded to feed its contemporaneous fliers (Lü et al., 2010a), which include pterosaurs (Lü et al., 2006; Lü,2009), feathered maniraptorans (Czerkas and Yuan 2002; Zhang et al. 2002; Xu et al. 2009) and gliding mammals (Meng et al., 2006). The broad mouth and peg-like teeth in Jeholopterus and Dendrorhynchoides (=Dendrorhynchus) curvidentatus (Ji and Ji, 1998; Ji et al., 1999) indicate that these animals were probably insectivorous, just like Anurognathus and Batrachognathus (Wellnhofer and Kellner, 1991). The teeth of Liaoxipterus are rhombic with moderately sharp tips, they are different from the much longer, slenderer teeth with sharp tips of the fish-eating pterosaurs, such as Rhamphorhynchus (Wellnhofer, 1991), Feilongus (Wang et al., 2005), Boreaopterus (Lü and Ji, 2005), and Zhenyuanopterus (Lü, 2010b). The tooth morphology plus the complete hyoid apparatus of Liaoxipterus may provide the possible evidence to support its insect-eating behavior.

3　Conclusion

The long processus lingualis (processus entoglossus) of the hyoid apparatus (Colbert, 1945; Romer, 1956) indicates that Liaoxipterus may have practiced lingual feeding behavior, similar to the modern reptile Chamelon (Kardong, 1998). This may be an evidence to support lingual feeding behavior of pterosaurs, and it also implies that Liaoxipterus is an insect-eating pterosaur rather than a fish-eating pterosaur.

Acknowledgements: I am indebted to Professors Louis Jacobs (Southern Methodist University, USA) and Philip Currie (University of Alberta, Canada), who read the first draft of this paper and made constructive suggestions, and to Dr. Dale Winkler (Southern Methodist University, USA) for his help in different ways. This research was supported by grants from the National Natural Science Foundation of China (grant no.:41272022) and the China Geological Survey (grant no.12120114026801) to Lü Jun-chang.

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The Hyoid Apparatus of Liaoxipterus Brachycephalus (Pterosauria) and Its Implications for Food-catching Behavior

Lü Jun-chang
Institute of Geology, Chinese Academy of Geological Sciences, Beijing 100037; Key Lab of Stratigraphy and Paleontology, Ministry of Land and Resources of China, Beijing 100037

The feeding behavior of pterosaurs was varied in different groups. Judging by the tooth morphologies and fossilized stomach contents of pterosaurs, the feeding habits included fish-eating, insect-eating, filtering small aquatic organisms, eating shelled crabs and snails, and fruit-eating. Because of the need for survival, they occupied different ecological niches, which determined their different food sources. Herein described is an almost complete, well-preserved hyoid apparatus of Liaoxipterus brachyognathus in comparison with the hyoid apparatus of the modern lizard Chameleon. The long processus lingualis (processus entoglossus) is similar to that of the modern lizard Chameleon, which captures prey by tongue, implying that Liaoxipterus might share a similar lingual feeding behavior. This phenomenon, plus its special tooth morphology, further suggests that it was an insect-eating rather than fish-eating pterosaur.

hyoid apparatus; Liaoxipterus; pterosauria; China

Q915.2; Q915.86

A

10.3975/cagsb.2015.03.13

本文由國家自然基金(編號: 41272022)和中國地質(zhì)調(diào)查局地質(zhì)調(diào)查項目(編號: 12120114026801)聯(lián)合資助。

2015-03-09; 改回日期: 2015-04-01。責任編輯: 閆立娟。

呂君昌, 男, 1965年生。研究員, 博士生導師。主要從事中生代爬行動物(尤其是恐龍類和翼龍類)及其地層學研究。通訊地址: 100037, 北京市西城區(qū)百萬莊大街26號。電話: 010-68999707。E-mail: Lujc2008@126.com。