Thomas Kleinteich

The filter pads and filtration mechanisms of the devil rays: Variation at macro and microscopic scales

Three lineages of cartilaginous fishes have independently evolved filter feeding (Lamniformes: Megachasma and Cetorhinus, Orectolobiformes: Rhincodon, and Mobulidae: Manta and Mobula); and the structure of the branchial filters is different in each group. The filter in Rhincodon typus has been described; species within the Lamniformes have simple filamentous filters, but the anatomy and ultrastructure of the branchial filter in the mobulid rays varies and is of functional interest. In most fishes, branchial gill rakers are elongated structures located along the anterior ceratobranchial and/or epibranchial arches; however, mobulid gill rakers are highly modified, flattened, lobe‐like structures located on the anterior and posterior epibranchial elements as well as the ceratobranchials. The ultrastructure of the filter lobes can be smooth or covered by a layer of microcilia, and some are denticulated along the dorsal and ventral lobe surface. Flow through the mobulid oropharyngeal cavity differs from other filter‐feeding fishes in that water must rapidly deviate from the free stream direction. There is an abrupt 90° turn from the initial inflowing path to move through the laterally directed branchial filter pores, over the gill tissue, and out the ventrally located gill slits. The deviation in the flow must result in tangential shearing stress across the filter surface. This implies that mobulids can use cross‐flow filtration in which this shearing force serves as a mechanism to resuspend food particles initially caught by sieving or another capture mode. These particles will be transported by the cross filter flow toward the esophagus. We propose that species with cilia on the rakers augment the shear mediated movement of particles along the filter with ciliary transport. J. Morphol. 274:1026–1043, 2013.

Stick tight: suction adhesion on irregular surfaces in the northern clingfish

The northern clingfish, Gobiesox maeandricus, is able to adhere to slippery, fouled and irregular surfaces in the marine intertidal environment. We have found that the fish can adhere equally well to surfaces with a broad range of surface roughness, from the finest sandpaper (Ra = 15 µm) to textures suitable for removing finish from flooring (Ra = 269 µm). The fishes outperform man-made suction cups, which only adhere to the smoothest surfaces. The adhesive forces of clingfish correspond to pressures 0.2–0.5 atm below ambient and are 80–230 times the body weight of the fish. The tenacity appears related to hierarchically structured microvilli around the edges of the adhesive disc that are similar in size and aspect ratio to the setae found on the feet of geckoes, spiders and insects. This points to a possible biomimetic solution to the problem of reversibly adhering to irregular, submerged surfaces.

Structure and mechanical properties of Octopus vulgaris suckers

In this study, we investigate the morphology and mechanical features of Octopus vulgaris suckers, which may serve as a model for the creation of a new generation of attachment devices. Octopus suckers attach to a wide range of substrates in wet conditions, including rough surfaces. This amazing feature is made possible by the suckers tissues, which are pliable to the substrate profile. Previous studies have described a peculiar internal structure that plays a fundamental role in the attachment and detachment processes of the sucker. In this work, we present a mechanical characterization of the tissues involved in the attachment process, which was performed using microindentation tests. We evaluated the elasticity modulus and viscoelastic parameters of the natural tissues (E ∼ 10 kPa) and measured the mechanical properties of some artificial materials that have previously been used in soft robotics. Such a comparison of biological prototypes and artificial material that mimics octopus-sucker tissue is crucial for the design of innovative artificial suction cups for use in wet environments. We conclude that the properties of the common elastomers that are generally used in soft robotics are quite dissimilar to the properties of biological suckers.

Caecilian jaw-closing mechanics: integrating two muscle systems

Caecilians (Lissamphibia: Gymnophiona) are unique among vertebrates in having two sets of jaw-closing muscles, one on either side of the jaw joint. Using data from high-resolution X-ray radiation computed tomography scans, we modelled the effect of these two muscle groups (mm. levatores mandibulae and m. interhyoideus posterior) on bite force over a range of gape angles, employing a simplified lever arm mechanism that takes into account muscle cross-sectional area and fibre angle. Measurements of lever arm lengths, muscle fibre orientations and physiological cross-sectional area of cranial muscles were available from three caecilian species: Ichthyophis cf. kohtaoensis; Siphonops annulatus; and Typhlonectes natans. The maximal gape of caecilians is restricted by a critical gape angle above which the mm. levatores mandibulae will open the jaw and destabilize the mandibular joint. The presence of destabilizing forces in the caecilian jaw mechanism may be compensated for by a mandibular joint in that the fossa is wrapped around the condyle to resist dislocation. The caecilian skull is streptostylic; the quadrate–squamosal complex moves with respect to the rest of the skull. This increases the leverage of the jaw-closing muscles. We also demonstrate that the unusual jaw joint requires streptostyly because there is a dorsolateral movement of the quadrate–squamosal complex when the jaw closes. The combination of the two jaw-closing systems results in high bite forces over a wide range of gape angles, an important advantage for generalist feeders such as caecilians. The relative sizes and leverage mechanics of the two closing systems allow one to exert more force when the other has a poor mechanical advantage. This effect is seen in all three species we examined. In the aquatic T. natans, with its less well-roofed skull, there is a larger contribution of the mm. levatores mandibulae to total bite force than in the terrestrial I. cf. kohtaoensis and S. annulatus.

Packing a pinch: functional implications of chela shapes in scorpions using finite element analysis.

Scorpions depend on their pedipalps for prey capture, defense, mating and sensing their environment. Some species additionally use their pedipalps for burrowing or climbing. Because the pincers or chelae at the end of the pedipalps vary widely in shape, they have been used as part of a suite of characters to delimit ecomorphotypes. We here evaluate the influence of the different chela cuticular shapes on their performance under natural loading conditions. Chelae of 20 species, representing seven families and spanning most of the range of chela morphologies, were assigned to clusters based on chela shape parameters using hierarchical cluster analysis. Several clusters were identified corresponding approximately to described scorpion ecomorphotypes. Finite element models of the chela cuticulae were constructed from CT scans and loaded with estimated pinch forces based on in vivo force measurements. Chela shape clusters differed significantly in mean Von Mises stress and strain energy. Normalized FEA showed that chela shape significantly influenced Von Mises stress and strain energy in the chela cuticula, with Von Mises stress varying up to an order of magnitude and strain energy up to two orders of magnitude. More elongate, high‐aspect ratio chela forms showed significantly higher mean stress compared with more robust low‐aspect ratio forms. This suggests that elongate chelae are at a higher risk of failure when operating near the maximum pinch force. Phylogenetic independent contrasts (PIC) were calculated based on a partly resolved phylogram with branch lengths based on an alignment of the 12S, 16S and CO1 mitochondrial genes. PIC showed that cuticular stress and strain in the chela were correlated with several shape parameters, such as aspect ratio, movable finger length, and chela height, independently of phylogenetic history. Our results indicate that slender chela morphologies may be less suitable for high‐force functions such as burrowing and defense. Further implications of these findings for the ecology and evolution of the different chela morphologies are discussed.

The hyal and ventral branchial muscles in caecilian and salamander larvae: homologies and evolution.

Amphibians (Lissamphibia) are characterized by a bi‐phasic life‐cycle that comprises an aquatic larval stage and metamorphosis to the adult. The ancestral aquatic feeding behavior of amphibian larvae is suction feeding. The negative pressure that is needed for ingestion of prey is created by depression of the hyobranchial apparatus as a result of hyobranchial muscle action. Understanding the homologies of hyobranchial muscles in amphibian larvae is a crucial step in understanding the evolution of this important character complex. However, the literature mostly focuses on the adult musculature and terms used for hyal and ventral branchial muscles in different amphibians often do not reflect homologies across lissamphibian orders. Here we describe the hyal and ventral branchial musculature in larvae of caecilians (Gymnophiona) and salamanders (Caudata), including juveniles of two permanently aquatic salamander species. Based on previous alternative terminology schemes, we propose a terminology for the hyal and ventral branchial muscles that reflects the homologies of muscles and that is suited for studies on hyobranchial muscle evolution in amphibians. We present a discussion of the hyal and ventral branchial muscles in larvae of the most recent common ancestor of amphibians (i.e. the ground plan of Lissamphibia). Based on our terminology, the hyal and ventral branchial musculature of caecilians and salamanders comprises the following muscles: m. depressor mandibulae, m. depressor mandibulae posterior, m. hyomandibularis, m. branchiohyoideus externus, m. interhyoideus, m. interhyoideus posterior, m. subarcualis rectus I, m. subarcualis obliquus II, m. subarcualis obliquus III, m. subarcualis rectus II‐IV, and m. transversus ventralis IV. Except for the m. branchiohyoideus externus, all muscles considered herein can be assigned to the ground plan of the Lissamphibia with certainty. The m. branchiohyoideus externus is either apomorphic for the Batrachia (frogs + salamanders) or salamander larvae depending on whether or not a homologous muscle is present in frog tadpoles. J. Morphol., 2011.

Landing on branches in the frog Trachycephalus resinifictrix (Anura: Hylidae)

Frogs (Lissamphibia: Anura) are famous for their saltatory or hopping locomotion, which is related to numerous anatomical specialisations that are characteristic for the group. However, while the biomechanics of take-off in frogs have been studied in detail, much less is known on how frogs land after a jump. Besides terrestrial and aquatic species, several lineages of frogs adopted an arboreal lifestyle and especially the biomechanics of landing on challenging, small, and unpredictable substrates, such as leaves or branches, are virtually unknown. Here we studied the landing kinematics of the arboreal frog Trachycephalus resinifictrix (Hylidae) on a wooden stick that was used to mimic a small tree branch. We observed two different landing behaviours: (1) landing on the abdomen and (2) attachment with the toes of either the forelimb or the hindlimb. In the latter case, the frogs performed a cartwheel around the stick, while they were only attached by their adhesive toe pads. We estimated the forces that act on the toes during this behaviour to be up to fourteen times the body weight of the animals. This behaviour demonstrates the remarkable adhesive capabilities of the toe pads and the body control of the frogs.

Is solid always best? Cranial performance in solid and fenestrated caecilian skulls.

SUMMARY Caecilians (Lissamphibia: Gymnophiona) are characterized by a fossorial lifestyle that appears to play a role in the many anatomical specializations in the group. The skull, in particular, has been the focus of previous studies because it is driven into the substrate for burrowing. There are two different types of skulls in caecilians: (1) stegokrotaphic, where the squamosal completely covers the temporal region and the jaw closing muscles, and (2) zygokrotaphic, with incomplete coverage of the temporal region by the squamosal. We used 3-D imaging and modeling techniques to explore the functional consequences of these skull types in an evolutionary context. We digitally converted stegokrotaphic skulls into zygokrotaphic skulls and vice versa. We also generated a third, akinetic skull type that was presumably present in extinct caecilian ancestors. We explored the benefits and costs of the different skull types under frontal loading at different head angles with finite element analysis (FEA). Surprisingly, the differences in stress distributions and bending between the three tested skull types were minimal and not significant. This suggests that the open temporal region in zygokrotaphic skulls does not lead to poorer performance during burrowing. However, the results of the FEA suggest a strong relationship between the head angle and skull performance, implying there is an optimal head angle during burrowing.

Frog tongue acts as muscle-powered adhesive tape

Frogs are well known to capture fast-moving prey by flicking their sticky tongues out of the mouth. This tongue projection behaviour happens extremely fast which makes frog tongues a biological high-speed adhesive system. The processes at the interface between tongue and prey, and thus the mechanism of adhesion, however, are completely unknown. Here, we captured the contact mechanics of frog tongues by filming tongue adhesion at 2000 frames per second through an illuminated glass. We found that the tongue rolls over the target during attachment. However, during the pulling phase, the tongue retractor muscle acts perpendicular to the target surface and thus prevents peeling during tongue retraction. When the tongue detaches, mucus fibrils form between the tongue and the target. Fibrils commonly occur in pressure-sensitive adhesives, and thus frog tongues might be a biological analogue to these engineered materials. The fibrils in frog tongues are related to the presence of microscopic papillae on the surface. Together with a layer of nanoscale fibres underneath the tongue epithelium, these surface papillae will make the tongue adaptable to asperities. For the first time, to the best of our knowledge, we are able to integrate anatomy and function to explain the processes during adhesion in frog tongues.

Applying X-ray tomography in the field of vertebrate biology: form, function, and evolution of the skull of caecilians (Lissamphibia: Gymnophiona)

Evolutionary research in biology relies on the comparison of different individuals of different species in order to explore the history of todays biodiversity. Synchrotron radiation based high resolution X-ray tomography (SRμCT) rapidly generates detailed three dimensional datasets. At the beamlines W2 and BW2 of the storage ring DORIS at DESY, Hamburg, Germany, we used SRμCT to study the cranial anatomy of different species and different developmental stages of caecilians (Lissamphibia: Gymnophiona). Here we describe a work-flow for analysis of the SRμCT data that covers segmentation of tissues in Amira® (Mercury Computer Systems), photorealistic rendering and animation in MayaTM, rapid prototyping, and morphometrics. The integration of different analyses of SRμCT data in our study resulted in a comprehensive understanding of form, function, and evolution of caecilian skulls. SRμCT imaging has the potential to become a standard technique for life sciences applications in the near future.