Department of Integrative Zoology, University of Vienna, Vienna, Austria.
PLoS One. 2012;7(9):e46344. doi: 10.1371/journal.pone.0046344. Epub 2012 Sep 28.
The oropharynx as a functional entity plays a fundamental role in feeding. Transitions from aquatic to terrestrial lifestyles in vertebrates demanded major changes of the oropharynx for the required adaptations to a different feeding environment. Extant turtles evolved terrestrial feeding modes in three families (testudinids, emydids, geoemydids)-independently from other amniotes-and are therefore important model organisms to reconstruct morpho-functional changes behind aquatic-terrestrial transitions. In this study we hypothesized that the oropharyngeal morphology in semiaquatic turtles of the geoemydid family shows parallels to testudinids, the only purely terrestrial extant lineage. We provide an in-depth description of the oropharynx in the semiaquatic geoemydid Heosemys grandis by using a combination of micro computed tomography (micro-CT) and subsequent digital in situ 3-D reconstruction, scanning electron microscopy (SEM), and histology. We show that H. grandis has a large tongue with rough papillose surface and well-developed lingual muscles. The attachment sites of the lingual muscles on the hyolingual skeleton and their courses within the tongue are nearly identical with testudinids. The hyolingual skeleton itself is mainly cartilaginous and shows distinct-but compared to testudinids rather small-anterior extensions of the hyoid body and hypoglossum. Oral glands are well developed in H. grandis but are smaller and simpler than in testudinids. Similarly, oropharyngeal keratinization was minimal and found only in the anterior palate, regions close to the beak, and tongue tip. We conclude that H. grandis shows distinct oropharyngeal morpho-functional adaptations for a terrestrial lifestyle but still retains characters typical for aquatic forms. This makes this species an important example showing the oropharyngeal adaptations behind aquatic-terrestrial transitions in turtles.
咽作为一个功能实体，在进食中起着至关重要的作用。脊椎动物从水生生活方式向陆生生活方式的转变，要求咽发生重大变化，以适应不同的进食环境。现存的海龟在三个科（龟鳖目、鳖科、曲颈龟亚目）中独立进化出了陆生进食方式，因此是重建水生-陆生过渡背后形态功能变化的重要模式生物。在这项研究中，我们假设半水生鳖科海龟的咽形态与唯一纯粹的陆生现存谱系——龟鳖目相似。我们通过结合微计算机断层扫描（micro-CT）和随后的数字原位 3D 重建、扫描电子显微镜（SEM）和组织学，对半水生鳖科的地龟进行了咽的深入描述。我们表明，地龟有一个大舌头，表面有粗糙的乳头状突起，并且舌肌发达。舌肌在咽骨上的附着点及其在舌内的走行与龟鳖目几乎相同。咽骨本身主要是软骨，与龟鳖目相比，有明显的但相对较小的舌骨体和舌下骨的前伸部。地龟的口腔腺发达，但比龟鳖目小而简单。同样，咽的角质化程度很低，只在前腭、靠近喙的区域和舌的尖端发现。我们得出结论，地龟表现出明显的适应陆地生活方式的咽形态功能，但仍保留了水生形态的特征。这使得该物种成为一个重要的例子，展示了海龟在水生-陆生过渡背后的咽适应。
