Structure and function of the feeding apparatus in the common musk turtle Sternotherus odoratus (Chelonia, Kinosternidae)

Natchev, Nikolay; Heiss, Egon; Singer, Katharina; Kummer, Stefan; Salaberger, Dietmar; Weisgram, Josef

doi:10.1163/18759866-08002004

Cited by 13 publications

(23 citation statements)

References 43 publications

(61 reference statements)

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“…However, most extant turtles cannot generate such strong suction flows and only compensate (“gulp”) the bow wave that otherwise would push small to moderately sized food items away from the fast approaching head. These species finally fix and grasp prey with the jaws (see Lauder & Prendergast, 1992 ; Lemell, Beisser & Weisgram, 2000 ; Aerts, Van Damme & Herrel, 2001 ; Natchev et al, 2009 ; Natchev et al, 2011 ). We consider the latter plesiomorphic behaviour for extant turtles.…”

Section: Discussionmentioning

confidence: 99%

Feeding behaviour in a ‘basal’ tortoise provides insights on the transitional feeding mode at the dawn of modern land turtle evolution

Natchev

Tzankov

Werneburg

et al. 2015

PeerJ

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Almost all extant testudinids are highly associated with terrestrial habitats and the few tortoises with high affinity to aquatic environments are found within the genus Manouria. Manouria belongs to a clade which forms a sister taxon to all remaining tortoises and is suitable as a model for studying evolutionary transitions within modern turtles. We analysed the feeding behaviour of Manouria emys and due to its phylogenetic position, we hypothesise that the species might have retained some ancestral features associated with an aquatic lifestyle. We tested whether M. emys is able to feed both in aquatic and terrestrial environments. In fact, M. emys repetitively tried to reach submerged food items in water, but always failed to grasp them—no suction feeding mechanism was applied. When feeding on land, M. emys showed another peculiar behaviour; it grasped food items by its jaws—a behaviour typical for aquatic or semiaquatic turtles—and not by the tongue as generally accepted as the typical feeding mode in all tortoises studied so far. In M. emys, the hyolingual complex remained retracted during all food uptake sequences, but the food transport was entirely lingual based. The kinematical profiles significantly differed from those described for other tortoises and from those proposed from the general models on the function of the feeding systems in lower tetrapods. We conclude that the feeding behaviour of M. emys might reflect a remnant of the primordial condition expected in the aquatic ancestor of the tortoises.

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Section: Discussionmentioning

confidence: 99%

Feeding behaviour in a ‘basal’ tortoise provides insights on the transitional feeding mode at the dawn of modern land turtle evolution

Natchev

Tzankov

Werneburg

et al. 2015

PeerJ

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“…One such mechanism-related feature is found in the hyoid corpus, or the central element of the hyobranchial apparatus. Suction-feeding jawed vertebrates have an ossified hyoid corpus that rigidly integrates with the right and left hyoid horns, in whales [50], turtles [19], [24], [42], [51], and sharks (TT pers. obs.…”

Section: Mechanically Important Hard-tissue Featuresmentioning

confidence: 99%

“…2). It was specifically stated [24] that the absence of an ossified hyoid corpus in Sternotherus impaired the suction ability of this turtle. This is mechanically expected because the hyoid corpus is the central element of the hyobranchial apparatus that maintains its integrity and rigidity.…”

Section: Mechanically Important Hard-tissue Featuresmentioning

confidence: 99%

“…Taxa: a, Mata Mata Turtle Chelus fimbriatus ; b, Japanese Angel Shark Squatina japonica ; c, Pygmy Sperm Whale Kogia breviceps ; d, Common Musk Turtle Sternotherus odoratus ; e, Sharpnose Sevengill Shark Heptranchias perlo ; f, Bottlenose Dolphin Tursiops truncatus; and g, Triassic Ichthyosaur Qianichthyosaurus zhoui . Derivations: a based [19]; b and e from CT data; c and f based on [52]; d based on [24]; and g based on IVPP 11838. Not to scale.…”

Section: Mechanically Important Hard-tissue Featuresmentioning

confidence: 99%

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Absence of Suction Feeding Ichthyosaurs and Its Implications for Triassic Mesopelagic Paleoecology

Motani

Tomita

et al. 2013

PLoS ONE

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Mesozoic marine reptiles and modern marine mammals are often considered ecological analogs, but the extent of their similarity is largely unknown. Particularly important is the presence/absence of deep-diving suction feeders among Mesozoic marine reptiles because this would indicate the establishment of mesopelagic cephalopod and fish communities in the Mesozoic. A recent study suggested that diverse suction feeders, resembling the extant beaked whales, evolved among ichthyosaurs in the Triassic. However, this hypothesis has not been tested quantitatively. We examined four osteological features of jawed vertebrates that are closely linked to the mechanism of suction feeding, namely hyoid corpus ossification/calcification, hyobranchial apparatus robustness, mandibular bluntness, and mandibular pressure concentration index. Measurements were taken from 18 species of Triassic and Early Jurassic ichthyosaurs, including the presumed suction feeders. Statistical comparisons with extant sharks and marine mammals of known diets suggest that ichthyosaurian hyobranchial bones are significantly more slender than in suction-feeding sharks or cetaceans but similar to those of ram-feeding sharks. Most importantly, an ossified hyoid corpus to which hyoid retractor muscles attach is unknown in all but one ichthyosaur, whereas a strong integration of the ossified corpus and cornua of the hyobranchial apparatus has been identified in the literature as an important feature of suction feeders. Also, ichthyosaurian mandibles do not narrow rapidly to allow high suction pressure concentration within the oral cavity, unlike in beaked whales or sperm whales. In conclusion, it is most likely that Triassic and Early Jurassic ichthyosaurs were ‘ram-feeders’, without any beaked-whale-like suction feeder among them. When combined with the inferred inability for dim-light vision in relevant Triassic ichthyosaurs, the fossil record of ichthyosaurs does not suggest the establishment of modern-style mesopelagic animal communities in the Triassic. This new interpretation matches the fossil record of coleoids, which indicates the absence of soft-bodied deepwater species in the Triassic.

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“…Turtles also possess a "hard palate" consisting of expanded palatine and maxillary bones, fusing in the midline just posterior to the choanae and articulating with the cranial base posteriorly (Gaffney,'79). They utilize their palates as a food-processing and prey handling surface (Natchev et al, 2010(Natchev et al, , 2011Parham and Pyenson, 2010). Additionally, ancient turtles such as Kayentachelys, Proterochersis, Proganochelys, and Odontochelys possessed marginal as well as palatine teeth (Li et al, 2008;Davit-Beal et al, 2009), which were lost during evolution, possibly due to changes in diet or habitat.…”

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confidence: 99%

Divergent palate morphology in turtles and birds correlates with differences in proliferation and BMP2 expression during embryonic development

2013

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During embryonic development, amniotes typically form outgrowths from the medial sides of the maxillary prominences called palatal shelves or palatine processes. In mammals the shelves fuse in the midline and form a bony hard palate that completely separates the nasal and oral cavities. In birds and lizards, palatine processes develop but remain unfused, leaving a natural cleft. Adult turtles do not possess palatine processes and unlike other amniotes, the internal nares open into the oral cavity. Here we investigate craniofacial ontogeny in the turtle, Emydura subglobosa to determine whether vestigial palatine processes develop and subsequently regress, or whether development fails entirely. We found that the primary palate in turtles develops similarly to other amniotes, but secondary palate ontogeny diverges. Using histology, cellular dynamics and in situ hybridization we found no evidence of palatine process development at any time during ontogeny of the face in the turtle. Furthermore, detailed comparisons with chicken embryos (the model organism most closely related to turtles from a molecular phylogeny perspective), we identified differences in proliferation and gene expression patterns that correlate with the differences in palate morphology. We propose that, in turtles, palatine process outgrowth is never initiated due to a lack of mesenchymal bone morphogenetic protein 2 (BMP2) expression in the maxillary mesenchyme, which in turn fails to induce the relatively higher cellular proliferation required for medial tissue outgrowth. It is likely that these differences between turtles and birds arose after the divergence of the lineage leading to modern turtles.

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Structure and function of the feeding apparatus in the common musk turtle Sternotherus odoratus (Chelonia, Kinosternidae)

Cited by 13 publications

References 43 publications

Feeding behaviour in a ‘basal’ tortoise provides insights on the transitional feeding mode at the dawn of modern land turtle evolution

Feeding behaviour in a ‘basal’ tortoise provides insights on the transitional feeding mode at the dawn of modern land turtle evolution

Absence of Suction Feeding Ichthyosaurs and Its Implications for Triassic Mesopelagic Paleoecology

Divergent palate morphology in turtles and birds correlates with differences in proliferation and BMP2 expression during embryonic development

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