Phenotypic flexibility of gape anatomy fine-tunes the aquatic prey-capture system of newts

A unique example of phenotypic flexibility of the oral apparatus is present in newts (Salamandridae) that seasonally change between an aquatic and a terrestrial habitat. Newts grow flaps of skin between their upper and lower jaws, the labial lobes, to partly close the corners of the mouth when they adopt an aquatic lifestyle during their breeding season. Using hydrodynamic simulations based on mu CT-scans and cranial kinematics during prey-capture in the smooth newt (Lissotriton vulgaris), we showed that this phenotypic flexibility is an adaptive solution to improve aquatic feeding performance: both suction distance and suction force increase by approximately 15% due to the labial lobes. As the subsequent freeing of the corners of the mouth by resorption of the labial lobes is assumed beneficial for the terrestrial capture of prey by the tongue, this flexibility of the mouth fine-tunes the process of capturing prey throughout the seasonal switching between water and land

Functionality and plasticity of turtle-feeding with special emphasis on oropharyngeal structures

Ohne Zweifel spielt die Effizienz der Nahrungsaufnahme eine zentrale Rolle im Überlebenspotential einer Tierart. Schildkröten zeichnen sich nicht nur durch ein stammesgeschichtlich extrem hohes Alter, sondern auch durch eine bemerkenswerte ökologische Heterogenität aus. Sie beinhalten von rein wasserlebenden Formen bis hin zu Wüstenbewohnern alle erdenklichen Zwischenstufen. Diese Tatsache macht sie für die Erforschung der Evolution terrestrischer Lebensweisen in Tetrapoden besonders interessant, va. morphologische und kinematische Veränderungen in der Biologie der Nahrungsaufnahme betreffend. Frühere Studien an Tetrapoden – und speziell an Schildkröten – konnten einen Zusammenhang zwischen Phylogenie, Art der Nahrungsaufnahme und oropharyngealer Morphologie aufzeigen. Morphologische Gegebenheiten erlauben bestimmte Arten der Nahrungsaufnahme, bzw. limitieren andere. Eine rein aquatische Schildkröte z.B. kann keine Nahrung an Land aufnehmen, genauso wie eine rein terrestrische Schildkröte nicht mehr unter Wasser fressen kann. Da alle heute lebenden Schildkröten von aquatischen Formen abstammen, muss die terrestrische Lebensweise dieser Ordnung sekundär entstanden sein. In diesem Zusammenhang werden in der vorliegenden Studie die Morphologie des oropharyngealen Systems, genauso wie das Fressverhalten und daraus resultierende kinematische Profile fünf selektierter Schildkrötenarten vergleichend untersucht. Bei den ausgesuchten Arten handelt es sich um die rein aquatische Sternotherus odoratus, drei amphibisch lebenden Cuora-Arten (Cuora amboinensis, C. flavomarginata, C. galbinifrons) und die terrestrische Art Manouria emys. Mit Hilfe mikro- und makroanatomische Verfahren wie Sektion, Histologie, Rasterelektronenmikroskopie (SEM) und Computertomographie konnten detaillierte morphologische Beschreibungen, genauso wie funktionelle Vergleiche erstellt werden. Dabei konnte gezeigt werden, dass der Bauplan des Nahrungsaufnahme-Apparates sich nicht nur bei weit entfernt verwandten Arten stark voneinander unterscheidet (z.B. S. odoratus vs. M. emys), sondern große Unterschiede auch innerhalb nur einer Gattung vorkommen (Cuora sp.) können. Diese interspezifische Plastizität im Design des Nahrungsaufnahme-Apparates spiegelt die Anpassung der Arten an unterschiedliche trophische Nischen wieder und erlaubt auch ein Erkennen von mikro- und makroanatomischen Mustern, welche im Laufe der Evolution der terrestrischen Lebensweise aus funktioneller Notwendigkeit entstanden sind. Analog zu den morphologischen Unterschieden konnten durch die Analyse von high-speed-Filmaufnahmen auch klare Abweichungen im Verhalten und kinematischen Profil zwischen den Arten bei der Nahrungsaufnahme gezeigt werden. So kann die Schildkröte S. odoratus (Familie Kinosternidae) zwar an Land Futterstücke mit den Kiefern ergreifen, um den gesamten Fressvorgang vollenden zu können ist diese Art aber auf ein aquatisches Milieu angewiesen. Die amphibisch lebenden Cuora Arten (Familie Geoemydidae) hingegen sind sehr gut sowohl an ein aquatisches wie auch terrestrisches Milieu angepasst und sind befähigt in beiden Medien Nahrung aufzunehmen, auch wenn innerhalb des Cuora Arten-Komplexes verschiedene Habitatpräferenzen festzustellen sind. Im Gegensatz dazu hat die terrestrische Schildkrötenart M. emys im Laufe der Evolution ihre Fähigkeit verloren unter Wasser zu fressen, auch wenn ihre Lebensweise noch stark amphibischen Charakter aufweißt. Die in dieser Studie erzielten Ergebnisse deuten darauf hin, dass selbst kleine Veränderung in der Morphologie des Nahrungsaufnahmeapparates große Veränderungen in seiner Funktion mit sich bringen können, was u. U. zu ökologischen Verschiebungen („ecological shifts“) führen kann. Folglich wird gezeigt dass eine Verschiebung von primär aquatischer- hin zu primär terrestrischer Lebensweise in modernen Schildkröten mindestens dreimal unabhängig voneinander entstanden ist. Schlussendlich erlaubt der intermediäre Charakter der untersuchten Schildkrötenarten eine stufenweise Rekonstruktion evolutionärer Vorgänge, die im Laufe der Veränderung von aquatischen bis hin zu terrestrischen Schildkröten stattgefunden haben – basierend auf der Evolution einer terrestrischen Nahrungsaufnahme.Feeding plays a critical role in survival, making the contribution of the feeding system to fitness substantial. As turtles show a great diversity in their ecology – they span the range from fully aquatic to fully terrestrial with all possible variations in between – they are especially interesting for studying morphological, kinematic, and behavioural changes that have been taken place during the transition from water to land in tetrapod evolution. Previous studies on aquatic and terrestrial turtles showed a correlation between phylogeny, feeding mode, and oropharyngeal morphology. This means that the oropharyngeal anatomy both enables and constrains the food uptake potential. A purely aquatic turtle is therefore unable to feed on land, and a terrestrial turtle cannot take up food underwater. It is generally accepted that the ancestor of all living turtles was aquatic. Terrestrial feeding biology in extant turtles therefore is derived rather than ancestral. This study compares the oropharyngel morphology, feeding behaviour, and kinematic profiles of five extant turtle species. The five species represent one aquatic (Sternotherus odoratus), three amphibious (Cuora amboinensis, C. flavomarginata, C. galbinifrons) and one terrestrial (Manouria emys) form. Anatomical methods including dissection, histology, scanning electron microscopy (SEM), and computed tomography (CT) revealed that the design of the feeding apparatus differs considerably not only between distantly related species (e.g. S. odoratus vs. M. emys) but also within species of the same genus (Cuora sp.). This interspecific plasticity of the feeding apparatus reflects adaptations to various trophic niches. This also allows us to interpret the micro- and macro-anatomical patterns that have been taken place during the transition from an aquatic to a terrestrial lifestyle. Analogous to the differences in morphology, differences were also found in feeding behaviour and kinematics by analysing high-speed recordings. While the aquatic kinosternid S. odoratus can grasp food items on land but is unable to finalise feeding events out of the water, the geoemydid Cuora spp. are trophically well adapted to both environments, even if they show varying tendencies to one or the other medium. The testudinid M. emys by contrast is terrestrial and has lost the ability to take up food underwater, despite all efforts. The results of this study imply that even minor changes in the morphology of the feeding apparatus can lead to significant changes in its function, potentially resulting in ecological shifts. Consequently, a shift from aquatic to terrestrial or partly terrestrial lifestyle has developed at least three times independently amongst turtles. The intermediate character of the species selected for this study allow a theoretical step-by-step reconstruction model of the evolution of terrestrial lifestyle in turtles, based on the evolution of terrestrial feeding biology

A tongue for all seasons : extreme phenotypic flexibility in salamandrid newts

Many organisms faced with seasonally fluctuating abiotic and biotic conditions respond by altering their phenotype to account for the demands of environmental changes. Here we discovered that newts, which switch seasonally between an aquatic and terrestrial lifestyle, grow a complex adhesive system on their tongue pad consisting of slender lingual papillae and mucus-producing cells to increase the efficiency of prey capture as they move from water onto land. The adhesive system is reduced again as newts switch back to their aquatic stage, where they use suction to capture prey. As suction performance is also enhanced seasonally by reshaping of the mouth due to the growth of labial lobes, our results show that newts are exceptional in exhibiting phenotypic flexibility in two alternating components (i.e. tongue pad and labial lobes) within a single functional system, and suggest that this form of phenotypic flexibility demands complex genetic regulatio

Musculoskeletal architecture of the prey capture apparatus in salamandrid newts with multiphasic lifestyle: does anatomy change during the seasonal habitat switches?

Some newt species change seasonally between an aquatic and a terrestrial life as adults, and are therefore repeatedly faced with different physical circumstances that affect a wide range of functions of the organism. For example, it has been observed that seasonally habitat-changing newts display notable changes in skin texture and tail fin anatomy, allowing one to distinguish an aquatic and a terrestrial morphotype. One of the main functional challenges is the switch between efficient aquatic and terrestrial prey capture modes. Recent studies have shown that newts adapt quickly by showing a high degree of behavioral flexibility, using suction feeding in their aquatic stage and tongue prehension in their terrestrial stage. As suction feeding and tongue prehension place different functional demands on the prey capture apparatus, this behavioral flexibility may clearly benefit from an associated morphological plasticity. In this study, we provide a detailed morphological analysis of the musculoskeletal system of the prey capture apparatus in the two multiphasic newt species Ichthyosaura alpestris and Lissotriton vulgaris by using histological sections and micro-computed tomography. We then test for quantitative changes of the hyobranchial musculoskeletal system between aquatic and terrestrial morphotypes, The descriptive morphology of the cranio-cervical musculoskeletal system provides new insights on form and function of the prey capture apparatus in newts, and the quantitative approach shows hypertrophy of the hyolingual musculoskeletal system in the terrestrial morphotype of L.vulgaris but hypertrophy in the aquatic morphotype of I.alpestris. It was therefore concluded that the seasonal habitat shifts are accompanied by a species-dependent muscular plasticity of which the potential effect on multiphasic feeding performance in newts remains unclear

SnakeStrike: A Low-Cost Open-Source High-Speed Multi-Camera Motion Capture System

Current neuroethological experiments require sophisticated technologies to precisely quantify the behavior of animals. In many studies, solutions for video recording and subsequent tracking of animal behavior form a major bottleneck. Three-dimensional (3D) tracking systems have been available for a few years but are usually very expensive and rarely include very high-speed cameras; access to these systems for research is limited. Additionally, establishing custom-built software is often time consuming – especially for researchers without high-performance programming and computer vision expertise. Here, we present an open-source software framework that allows researchers to utilize low-cost high-speed cameras in their research for a fraction of the cost of commercial systems. This software handles the recording of synchronized high-speed video from multiple cameras, the offline 3D reconstruction of that video, and a viewer for the triangulated data, all functions previously also available as separate applications. It supports researchers with a performance-optimized suite of functions that encompass the entirety of data collection and decreases processing time for high-speed 3D position tracking on a variety of animals, including snakes. Motion capture in snakes can be particularly demanding since a strike can be as short as 50 ms, literally twice as fast as the blink of an eye. This is too fast for faithful recording by most commercial tracking systems and therefore represents a challenging test to our software for quantification of animal behavior. Therefore, we conducted a case study investigating snake strike speed to showcase the use and integration of the software in an existing experimental setup

Biomechanics and hydrodynamics of prey capture in the Chinese giant salamander reveal a high-performance jaw-powered suction feeding mechanism

During the evolutionary transition from fish to tetrapods, a shift from uni- to bidirectional suction feeding systems followed a reduction in the gill apparatus. Such a shift can still be observed during metamorphosis of salamanders, although many adult salamanders retain their aquatic lifestyle and feed by high-performance suction.Unfortunately, little is known about the interplay between jaws and hyobranchial motions to generate bidirectional suction flows. Here,we study the cranial morphology, aswell as kinematic and hydrodynamic aspects related to prey capture in the Chinese giant salamander (Andrias davidianus). Compared with fish and previously studied amphibians, A. davidianus uses an alternative suction mechanismthat mainly relies on accelerating water by separating the ‘plates’ formed by the long and broad upper and lower jaw surfaces. Computational fluid dynamics simulations, based on three-dimensional morphology and kinematical data from high-speed videos, indicate that the viscerocranial elements mainly serve to accommodate the water that was given a sufficient anterior-to-posterior impulse beforehand by powerful jawseparation.We hypothesize that this modifiedway of generating suction is primitive for salamanders, and that this behaviour could have played an important role in the evolution of terrestrial life in vertebrates by releasing mechanical constraints on the hyobranchial system

Ontogenetic Development of Weberian Ossicles and Hearing Abilities in the African Bullhead Catfish

BACKGROUND: The weberian apparatus of otophysine fishes facilitates sound transmission from the swimbladder to the inner ear to increase hearing sensitivity. It has been of great interest to biologists since the 19(th) century. No studies, however, are available on the development of the weberian ossicles and its effect on the development of hearing in catfishes. METHODOLOGY/PRINCIPAL FINDINGS: We investigated the development of the weberian apparatus and auditory sensitivity in the catfish Lophiobagrus cyclurus. Specimens from 11.3 mm to 85.5 mm in standard length were studied. Morphology was assessed using sectioning, histology, and X-ray computed tomography, along with 3D reconstruction. Hearing thresholds were measured utilizing the auditory evoked potentials recording technique. Weberian ossicles and interossicular ligaments were fully developed in all stages investigated except in the smallest size group. In the smallest catfish, the intercalarium and the interossicular ligaments were still missing and the tripus was not yet fully developed. Smallest juveniles revealed lowest auditory sensitivity and were unable to detect frequencies higher than 2 or 3 kHz; sensitivity increased in larger specimens by up to 40 dB, and frequency detection up to 6 kHz. In the size groups capable of perceiving frequencies up to 6 kHz, larger individuals had better hearing abilities at low frequencies (0.05-2 kHz), whereas smaller individuals showed better hearing at the highest frequencies (4-6 kHz). CONCLUSIONS/SIGNIFICANCE: Our data indicate that the ability of otophysine fish to detect sounds at low levels and high frequencies largely depends on the development of the weberian apparatus. A significant increase in auditory sensitivity was observed as soon as all weberian ossicles and interossicular ligaments are present and the chain for transmitting sounds from the swimbladder to the inner ear is complete. This contrasts with findings in another otophysine, the zebrafish, where no threshold changes have been observed

3D bite modeling and feeding mechanics of the largest living amphibian, the Chinese Giant Salamander Andrias davidianus (Amphibia:Urodela)

Biting is an integral feature of the feeding mechanism for aquatic and terrestrial salamanders to capture, fix or immobilize elusive or struggling prey. However, little information is available on how it works and the functional implications of this biting system in amphibians although such approaches might be essential to understand feeding systems performed by early tetrapods. Herein, the skull biomechanics of the Chinese giant salamander, Andrias davidianus is investigated using 3D finite element analysis. The results reveal that the prey contact position is crucial for the structural performance of the skull, which is probably related to the lack of a bony bridge between the posterior end of the maxilla and the anterior quadrato-squamosal region. Giant salamanders perform asymmetrical strikes. These strikes are unusual and specialized behavior but might indeed be beneficial in such sit-and-wait or ambush-predators to capture laterally approaching prey. However, once captured by an asymmetrical strike, large, elusive and struggling prey have to be brought to the anterior jaw region to be subdued by a strong bite. Given their basal position within extant salamanders and theirPeer ReviewedPostprint (published version

Dining dichotomy : aquatic and terrestrial prey capture behavior in the Himalayan newt Tylototriton verrucosus

Transitions between aquatic and terrestrial prey capture are challenging. Trophic shifts demand a high degree of behavioral flexibility to account for different physical circumstances between water and air to keep performance in both environments. The Himalayan newt, Tylototriton verrucosus, is mostly terrestrial but becomes aquatic during its short breeding period. Nonetheless, it was assumed that it lacks the capability of trophic behavioral flexibility, only captures prey on land by its tongue (lingual prehension) and does not feed in water. This theory was challenged from stomach content analyses in wild populations that found a variety of aquatic invertebrates in the newts' stomachs during their breeding season. Accordingly, we hypothesized that T. verrucosus actively changes its terrestrial prey capture mechanism to hunt for aquatic prey at least during its aquatic stage. In fact, the kinematic analyses showed that T. verrucosus uses lingual prehension to capture prey on land but changes to suction feeding for aquatic strikes. The statistical analyses revealed that terrestrial and aquatic strikes differ significantly in most kinematic parameters while behavioral variability does not differ between both behaviors. In turn, the movement patterns in suction feeding showed a higher degree of coordination between jaw and hyoid movements compared to the putative primary feeding mode, namely lingual prehension. We conclude that T. verrucosus, though relatively slow compared to trophic specialists, benefits from a high degree of behavioral flexibility that allows exploiting food sources efficiently from two very different habitats

The oropharyngeal morphology in the semiaquatic giant Asian pond turtle, heosemys grandis, and its evolutionary implications

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