Three-dimensional movement of the beak during seed processing in domestic canaries.

Many songbird species rely on seeds as a primary food source and the process of picking up, positioning, cracking, dehusking and swallowing seeds is one of the most sophisticated tasks of the beak. Still, we lack understanding about how granivorous songbirds move their beak during the different phases of seed processing. In this study, we used multi-view high-speed imaging to analyze the 3D movement of the beak in feeding domestic canaries. Our analysis focused on the correlation of the upper and lower beak, the frequency of mandibulation and the direction of mandible movement in 3D space. We show that the correlation of maxilla and mandible movement differs among the phases of seed processing. Furthermore, we found that the beak moves at extremely high frequencies, up to 25 Hz, which resembles previously reported maximal syllable rates in singing canaries. Finally, we report that canaries use specific 3D mandible movements during the different phases of seed processing. Kinematic parameters do not differ between male and female canaries. Our findings provide an important biomechanical basis for better understanding the beak as a functional tool.

Cranial kinesis facilitates quick retraction of stuck woodpecker beaks.

Much like nails that are hammered into wood, the beaks of woodpeckers regularly get stuck upon impact. A kinematic video analysis of pecking by black woodpeckers shows how they manage to quickly withdraw their beaks, revealing a two-phase pattern: first a few degrees of beak-tip-down rotation about the nasofrontal hinge causes the tip of the upper beak to be retruded while its proximal end is lifted. Next, the head is lifted, causing beak-tip-up rotation about the nasofrontal hinge while the lower beak starts retruding and initiates the final freeing. We hypothesise that these consecutive actions, taking place in about 0.05 s, facilitate beak retraction by exploiting the presumably low frictional resistance between the upper and lower beak keratin surfaces, allowing them to slide past each other. It also demonstrates the counter-intuitive value of maintaining cranial kinesis in a species adapted to deliver forceful impacts.

Unprecedented Biting Performance in Herbivorous Fish: How the Complex Biting System of Pomacentridae Circumvents Performance Trade-Offs.

AbstractIt is well accepted that the complexity of functional systems may mitigate performance trade-offs. However, data supporting this theory are hard to find because they need to be based on a functional system with different complexity levels in closely related species. The Pomacentridae (damselfishes) provide an excellent opportunity to test this hypothesis because most of the species have two mouth-closing systems: the first using the adductor mandibulae, as in all teleost fishes, and the second relying on the ceratomandibular (cmd) ligament, a synapomorphic trait of the family. Interestingly, some pomacentrids have secondarily lost the cmd ligament during evolution and therefore have a less complex mouth-closing system. Using dissection, kinematic analysis, and mathematical modeling, we demonstrated that the possession of two mouth-closing systems enabled grazing damselfishes to have a forceful and extremely fast bite. This combination challenges a major functional trade-off in fish jaw dynamics, as systems better suited for force transmission are usually less suited for speed transmission, and vice versa. The combination of grazing behavior, small and robust lower jaws (conferring high biting force), and an ultrafast bite is unusual within actinopterygians. These attributes and their associated performance seem to be required conditions to colonize the ecological niche of farming, that is, the maintenance of small filamentous algae crops serving as both food and storage.

Burrowing behaviour of the European eel (Anguilla anguilla): Effects of life stage.

The European eel (Anguilla anguilla) is a fascinating species, exhibiting a complex life cycle. The species is, however, listed as critically endangered on the IUCN Red List due to an amalgam of factors, including habitat loss. This study investigated the burrowing behaviour and substrate preference of glass, elver and yellow stages of A. anguilla. Preference was determined by introducing eels in aquaria with different substrates and evaluating the chosen substrate for burrowing. In addition, burrowing was recorded using a camera in all substrate types and analysed for kinematics. The experiments showed that all of these life stages sought refuge in the sediments with particle sizes ranging from sand to coarse gravel. Starting from a resting position, they shook their head horizontally in combination with rapid body undulations until half of their body was within the substrate. High-speed X-ray videography revealed that once partly in the sediment, eels used only horizontal head sweeps to penetrate further, without the use of their tail. Of the substrates tested, burrowing performance was highest in fine gravel (diameter 1-2 mm; lower burrowing duration, less body movements and/or lower frequency of movements), and all eels readily selected this substrate for burrowing. However, glass eels and elvers were able to use coarse gravel (diameter >8 mm) because their smaller size allowed manoeuvring through the spaces between the grains. Further, burrowing performance increased with body size: glass eels required more body undulations compared to yellow eels. Interestingly, the urge to hide within the sediment was highest for glass eels and elvers. Documentation of substrate preference and burrowing behaviour of A. anguilla provides new information about their potential habitat use. Considering that habitat alterations and deteriorations are partly responsible for the decline of the eel, this information can contribute to the development of more effective conservation measures.

Aquatic-terrestrial transitions of feeding systems in vertebrates: a mechanical perspective.

Transitions to terrestrial environments confront ancestrally aquatic animals with several mechanical and physiological problems owing to the different physical properties of water and air. As aquatic feeders generally make use of flows of water relative to the head to capture, transport and swallow food, it follows that morphological and behavioral changes were inevitably needed for the aquatic animals to successfully perform these functions on land. Here, we summarize the mechanical requirements of successful aquatic-to-terrestrial transitions in food capture, transport and swallowing by vertebrates and review how different taxa managed to fulfill these requirements. Amphibious ray-finned fishes show a variety of strategies to stably lift the anterior trunk, as well as to grab ground-based food with their jaws. However, they still need to return to the water for the intra-oral transport and swallowing process. Using the same mechanical perspective, the potential capabilities of some of the earliest tetrapods to perform terrestrial feeding are evaluated. Within tetrapods, the appearance of a mobile neck and a muscular and movable tongue can safely be regarded as key factors in the colonization of land away from amphibious habitats. Comparative studies on taxa including salamanders, which change from aquatic feeders as larvae to terrestrial feeders as adults, illustrate remodeling patterns in the hyobranchial system that can be linked to its drastic change in function during feeding. Yet, the precise evolutionary history in form and function of the hyolingual system leading to the origin(s) of a muscular and adhesive tongue remains unknown.

Angling-induced injuries have a negative impact on suction feeding performance and hydrodynamics in marine shiner perch, Cymatogaster aggregata.

Fishing is a popular and lucrative sport around the world and, in some cases, may contribute to declining fish stocks. To mediate this problem and maintain fish biomass in aquatic ecosystems, catch-and-release fishing, whereby a fish is caught and immediately released, has been implemented in many countries. It is unclear whether the injuries to the mouth that are caused by the hook have an impact on feeding performance of fishes. Using high-speed video and computational fluid dynamics (CFD), we asked whether injuries around the mouth caused by fishing hooks have a negative impact on suction feeding performance (measured as maximum prey velocity) of the commonly angled marine shiner perch (Cymatogaster aggregata). We hypothesized that fish with mouth injuries would exhibit decreased feeding performance compared with controls. Ten shiner perch were caught using scientific angling and 10 were caught using a seine net. Feeding events were then recorded at 500 frames per second using a high-speed camera. Compared with the control group, maximum prey velocity was significantly lower in the injured group (P<0.01). Maximum gape, time to peak gape, maximum jaw protrusion and predator-prey distance were comparable between the control and injured groups, leading us to conclude that the injury-induced hole in the buccal cavity wall reduced the pressure gradient during mouth expansion, thereby reducing the velocity of water entering the fish's mouth. This was confirmed with our CFD modelling. Fishing injuries in nature are likely to depress feeding performance of fish after they have been released, although it is currently unclear whether this has a significant impact on survival.

Kinematics of chisel-tooth digging by African mole-rats.

Mole-rats are known to use their protruding, chisel-like incisors to dig underground networks of tunnels, but it remains unknown how these incisors are used to break and displace the soil. Theoretically, different excavation strategies can be used. Mole-rats could either use their head depressor muscles to power scooping motions of the upper incisors (by nose-down head rotations) or the lower incisors (by nose-up head rotations), or their jaw adductors to grab and break the soil after penetrating both sets of incisors into the ground, or a combination of these mechanisms. To identify how chisel-tooth digging works, a kinematic analysis of this behaviour was performed based on high-speed videos of 19 individuals from the African mole-rat species Fukomys micklemi placed inside transparent tubes in a laboratory setting. Our analysis showed that the soil is penetrated by both the upper and lower incisors at a relatively high gape angle, generally with the head rotated nose-up. Initially, the upper incisors remain approximately stationary to function as an anchor to allow an upward movement of the lower incisors to grab the soil. Next, a quick, nose-down rotation of the head further detaches the soil and drops the soil below the head. Consequently, both jaw adduction and head depression are jointly used to power tooth-digging in F. micklemi The same mechanism, but with longer digging cycles, and soil being thrown down at smaller gape sizes, was used when digging in harder soil.

Unusual sound production mechanism in the triggerfish Rhinecanthus aculeatus (Balistidae).

The ability to produce sound has been known for decades in Balistidae. Sounds of many species have been recorded and a variety of sound-producing mechanisms have been proposed, including teeth stridulation, collision of the buccal teeth and movements of the fins. The best-supported hypothesis involves movements of the pectoral fin against the lateral part of the swimbladder, called a drumming membrane. In this study, we describe for the first time the sounds made by the blackbar triggerfish Rhinecanthus aculeatus, which are like short drum rolls with an average duration of 85 ms, 193 Hz dominant frequency and 136 dB SPL level at 3 cm distance. The sounds are a series of pulses that result from alternate sweeping movements of the right and left pectoral fins, which push a system of three scutes that are forced against the swimbladder wall. Pulses from each fin occur in consecutive pairs. High-speed videos indicate that each pulse consists of two cycles. The first part of each cycle corresponds to the inward buckling of the scutes, whereas the second part of the cycle corresponds to an apparent passive recoil of the scutes and swimbladder wall. This novel sound production mechanism is probably found in many members of Balistidae because these peculiar scutes occur in other species in the family. Comparison of sound characteristics from fishes of different sizes shows that dominant frequency decreases with size in juveniles but not in adults.

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.

Kinematics of mouthbrooding in Oreochromis niloticus (Cichlidae).

Many species from several different families of fishes perform mouthbrooding, where one of the sexes protects and ventilates the eggs inside the mouth cavity. This ventilation behaviour differs from gill ventilation outside the brooding period, as the normal, small-amplitude suction-pump respiration cycles are alternated with actions including near-simultaneous closed-mouth protrusions and high-amplitude depressions of the hyoid. The latter is called churning, referring to its hypothetical function in moving around and repositioning the eggs by a presumed hydrodynamic effect of the marked shifts in volume along the mouth cavity. We tested the hypothesis that churning causes the eggs located posteriorly in the mouth cavity to move anteriorly away from the gill entrance. This would prevent or clear accumulations of brood at the branchial basket, which would otherwise hinder breathing by the parent. Dual-view videos of female Nile tilapias (Oreochromis niloticus) during mouthbrooding showed that churning involves a posterior-to-anterior wave of expansion and compression of the head volume. Flow visualisation with polyethylene microspheres revealed a significant inflow of water entering the gill slits at the zone above the pectoral fin base, followed by a predominantly ventral outflow passing the ventrolaterally flapping branchiostegal membranes. X-ray videos indicated that particularly the brood located close to the gills is moved anteriorly during churning. These data suggest that, in addition to mixing of the brood to aid its oxygenation, an important function of the anterior flow through the gills and buccal cavity during churning is to prevent clogging of the eggs near the gills.

A fish that uses its hydrodynamic tongue to feed on land.

To capture and swallow food on land, a sticky tongue supported by the hyoid and gill arch skeleton has evolved in land vertebrates from aquatic ancestors that used mouth-cavity-expanding actions of the hyoid to suck food into the mouth. However, the evolutionary pathway bridging this drastic shift in feeding mechanism and associated hyoid motions remains unknown. Modern fish that feed on land may help to unravel the physical constraints and biomechanical solutions that led to terrestrialization of fish-feeding systems. Here, we show that the mudskipper emerges onto land with its mouth cavity filled with water, which it uses as a protruding and retracting 'hydrodynamic tongue' during the initial capture and subsequent intra-oral transport of food. Our analyses link this hydrodynamic action of the intra-oral water to a sequence of compressive and expansive cranial motions that diverge from the general pattern known for suction feeding in fishes. However, the hyoid motion pattern showed a remarkable resemblance to newts during tongue prehension. Consequently, although alternative scenarios cannot be excluded, hydrodynamic tongue usage may be a transitional step onto which the evolution of adhesive mucosa and intrinsic lingual muscles can be added to gain further independence from water for terrestrial foraging.

Functional morphology and kinematics of terrestrial feeding in the largescale foureyes (Anableps anableps).

A major challenge for aquatic vertebrates that invade land is feeding in the terrestrial realm. The capacity of the gape to become parallel with the ground has been shown to be a key factor to allow fishes to feed on prey lying on a terrestrial surface. To do so, two strategies have been identified that involve a nose-down tilting of the head: (1) by pivoting on the pectoral fins as observed in mudskippers, and (2) curling of the anterior part of the body supported by a long and flexible eel-like body as shown in eel-catfish. Although Anableps anableps successfully feeds on land, it does not possess an eel-like body or pectoral fins to support or lift the anterior part of the body. We identified the mechanism of terrestrial prey capture in A. anableps by studying kinematics and functional morphology of the cranial structures, using high-speed video and graphical 3D reconstructions from computed tomography scans. In contrast to the previously described mechanisms, A. anableps relies solely on upper and lower jaw movement for re-orientation of the gape towards the ground. The premaxilla is protruded anteroventrally, and the lower jaw is depressed to a right angle with the substrate. Both the lower and upper jaws are selectively positioned onto the prey. Anableps anableps thereby uses the jaw protrusion mechanism previously described for other cyprinodontiforms to allow a continued protrusion of the premaxilla even while closing the jaws. Several structural adaptations appear to allow more controlled movements and increased amplitude of anterior and ventral protrusion of the upper jaw compared with other cyprinodontiforms.

Suction power output and the inertial cost of rotating the neurocranium to generate suction in fish.

To expand the buccal cavity, many suction-feeding fishes rely on a considerable contribution from dorsal rotation of the dorsal part of the head including the brains, eyes, and several bones forming the braincase and skull roof (jointly referred to as the neurocranium). As the neurocranium takes up a large part of the total mass of the head, this rotation may incur a considerable inertial cost. If so, this would suggest a significant selective pressure on the kinematics and mass distribution of the neurocranium of suction feeders. Here, an inverse dynamic model is formulated to calculate the instantaneous power required to rotate the neurocranium, approximated by a quarter ellipsoid volume of homogeneous density, as well as to calculate the instantaneous suction power based on intra-oral pressure and head volume quantifications. We applied this model to largemouth bass (Micropterus salmoides) and found that the power required to rotate the neurocranium accounts for only about 4% of the power required to suck water into the mouth. Furthermore, recovery of kinetic energy from the rotating neurocranium converted into suction work may be possible during the phase of neurocranial deceleration. Thus, we suggest that only a negligible proportion of the power output of the feeding muscles is lost as inertial costs in the largemouth bass. Consequently, the feeding performance of piscivorous suction feeders with generalised morphology, comparable to our model species, is not limited by neurocranial motion during head expansion. This suggests that it is thus not likely to be a factor of importance in the evolution of cranial shape and size.

Flexibility is everything: prey capture throughout the seasonal habitat switches in the smooth newt Lissotriton vulgaris.

Transitions between aquatic and terrestrial habitats are significant steps in vertebrate evolution. Due to the different biophysical demands on the whole organism in water and air, such transitions require major changes of many physiological functions, including feeding. Accordingly, the capability to modulate the pre-programmed chain of prey-capture movements might be essential to maintain performance in a new environment. Newts are of special interest in this regard as they show a multiphasic lifestyle where adults change seasonally between an aquatic and a terrestrial stage. For instance, the Alpine newt is capable of using tongue prehension to feed on land only when in the terrestrial stage, but still manages to suction feed if immersed whilst in terrestrial stage. During the aquatic stage, terrestrial feeding always involved grasping prey by the jaws. Here, we show that this seasonal shift in feeding behavior is also present in a species with a shorter terrestrial stage, the smooth newt Lissotriton vulgaris. Behavioral variability increases when animals change from aquatic to terrestrial strikes in the aquatic stage, but prey-capture movements seem to be generally well-coordinated across the feeding modes. Only suction feeding in the terrestrial stage was seldom performed and appeared uncoordinated. Our results indicate that newts exhibit a high degree of seasonal flexibility of the prey-capture behavior. The similarity between movement patterns of suction feeding and terrestrial feeding suggests that only relatively subtle neuromotoric adjustments to the ancestral, suction-feeding motor program are required to successfully feed in the new environment.

New insights into the role of the pharyngeal jaw apparatus in the sound-producing mechanism of Haemulon flavolineatum (Haemulidae).

Grunts are fish that are well known to vocalize, but how they produce their grunting sounds has not been clearly identified. In addition to characterizing acoustic signals and hearing in the French grunt Haemulon flavolineatum, the present study investigates the sound-production mechanism of this species by means of high-speed X-ray videos and scanning electron microscopy of the pharyngeal jaw apparatus. Vocalizations consist of a series of stridulatory sounds: grunts lasting ~47 ms with a mean period of 155 ms and a dominant frequency of ~700 Hz. Auditory capacity was determined to range from 100 to 600 Hz, with greatest sensitivity at 300 Hz (105.0±11.8 dB re. 1 µPa). This suggests that hearing is not tuned exclusively to detect the sounds of conspecifics. High-speed X-ray videos revealed how pharyngeal jaws move during sound production. Traces of erosion on teeth in the fourth ceratobranchial arch suggest that they are also involved in sound production. The similarity of motor patterns of the upper and lower pharyngeal jaws between food processing and sound production indicates that calling is an exaptation of the food-processing mechanism.

Seed preference is only weakly linked to seed-type-specific feeding performance in a songbird.

The dehusking of seeds by granivorous songbirds is a complex process that requires fast, coordinated and sensory-feedback-controlled movements of beak and tongue. Hence, efficient seed handling requires a high degree of sensorimotoric skill and behavioural flexibility, since seeds vary considerably in size, shape and husk structure. To deal with this variability, individuals might specialise on specific seed types, which could result in greater seed handling efficiency of the preferred seed type, but lower efficiency for other seed types. To test this, we assessed seed preferences of canaries (Serinus canaria) through food choice experiments and related these to data of feeding performance, seed-handling skills and beak kinematics during feeding on small, spindle-shaped canary seeds and larger, spheroid-shaped hemp seeds. We found great variety in seed preferences among individuals: some had no clear preference, while others almost exclusively fed on hemp seeds, or even prioritized novel seed types (millet seed). Surprisingly, we only observed few and weak effects of seed preference on feeding efficiency. This suggests either that the ability to handle seeds efficiently can be readily applied across various seed types, or alternatively, that achieving high levels of seed-specific handling skills does not require extensive practice.

Masters of change: seasonal plasticity in the prey-capture behavior of the Alpine newt Ichthyosaura alpestris (Salamandridae).

Transitions between aquatic and terrestrial environments are significant steps in vertebrate evolution. These transitions require major changes in many biological functions, including food uptake and transport. The Alpine newt, Ichthyosaura alpestris, is known to show a 'multiphasic lifestyle' where the adult shifts from a terrestrial to an aquatic lifestyle and then back to a terrestrial lifestyle every year as a result of its breeding activity. These transitions correspond to dramatic changes in morphology, physiology and behavior, resulting in distinct aquatic and terrestrial morphotypes. We hypothesized that these shifts go along with changes in prey-capture mechanics to maintain a sufficiently high performance in both environments. We analyzed the prey-capture kinematics in the four possible modes: aquatic strikes in the aquatic phase, terrestrial strikes in the terrestrial phase, aquatic strikes in the terrestrial phase and terrestrial strikes in the aquatic phase. A multivariate comparison detected significant kinematic differences between the phase-specific feeding modes. In both the aquatic and the terrestrial phase, I. alpestris uses a suction-feeding mechanism for capturing prey in water. By contrast, I. alpestris uses a jaw-based grasping mechanism with a kinematic profile similar to the aquatic modes for terrestrial prey-capture in its aquatic phase but an elaborate lingual-based prehension mechanism to capture terrestrial prey in the terrestrial phase. These results exhibit a so-far unknown amount of behavioral plasticity in prey-capture behavior that is tuned to the seasonal demands of performance, and exemplify functional mechanisms behind aquatic-terrestrial transitions in vertebrates.

Mechanics of snout expansion in suction-feeding seahorses: musculoskeletal force transmission.

Seahorses and other syngnathid fishes rely on a widening of the snout to create the buccal volume increase needed to suck prey into the mouth. This snout widening is caused by abduction of the suspensoria, the long and flat bones outlining the lateral sides of the mouth cavity. However, it remains unknown how seahorses can generate a forceful abduction of the suspensoria. To understand how force is transmitted to the suspensoria via the hyoid and the lower jaw, we performed mathematical simulations with models based on computerized tomography scans of Hippocampus reidi. Our results show that the hinge joint between the left and right hyoid bars, as observed in H. reidi, allows for an efficient force transmission to the suspensorium from a wide range of hyoid angles, including the extremely retracted hyoid orientations observed in vivo for syngnathids. Apart from the hyoid retraction force by the sternohyoideus-hypaxial muscles, force generated in the opposite direction on the hyoid by the mandibulohyoid ligament also has an important contribution to suspensorium abduction torque. Forces on the lower jaw contribute only approximately 10% of the total suspensorium torque. In particular, when dynamical aspects of hyoid retraction are included in the model, a steep increase is shown in suspensorium abduction torque at highly retracted hyoid positions, when the linkages to the lower jaw counteract further hyoid rotation in the sagittal plane. A delayed strain in these linkages allows syngnathids to postpone suction generation until the end of cranial rotation, a fundamental difference from non-syngnathiform fishes.

Biomimetic models of fish gill rakers as lateral displacement arrays for particle separation.

Ram suspension-feeding fish, such as herring, use gill rakers to separate small food particles from large water volumes while swimming forward with an open mouth. The fish gill raker function was tested using 3D-printed conical models and computational fluid dynamics simulations over a range of slot aspect ratios. Our hypothesis predicting the exit of particles based on mass flow rates, dividing streamlines (i.e. stagnation streamlines) at the slots between gill rakers, and particle size was supported by the results of experiments with physical models in a recirculating flume. Particle movement in suspension-feeding fish gill raker models was consistent with the physical principles of lateral displacement arrays ('bump arrays') for microfluidic and mesofluidic separation of particles by size. Although the particles were smaller than the slots between the rakers, the particles skipped over the vortical region that was generated downstream from each raker. The particles 'bumped' on anterior raker surfaces during posterior transport. Experiments in a recirculating flume demonstrate that the shortest distance between the dividing streamline and the raker surface preceding the slot predicts the maximum radius of a particle that will exit the model by passing through the slot. This theoretical maximum radius is analogous to the critical separation radius identified with reference to the stagnation streamlines in microfluidic and mesofluidic devices that use deterministic lateral displacement and sieve-based lateral displacement. These conclusions provide new perspectives and metrics for analyzing cross-flow and cross-step filtration in fish with applications to filtration engineering.