France

Recent application of biplanar videoradiography and the XROMM workflow to the study of hyolingual kinematics in primates provides new insight into tongue movements during chewing and swallowing. During chewing in macaques, during fast open and fast close the molar region of the tongue rolls to the chewing side simultaneously with sagittal flexion. Twisting and flexion reach their maxima early in the fast close phase of chewing cycles, positioning the food bolus between the approaching teeth prior to the power stroke. Nerve block of tactile sensation from trigeminal innervated oral structures decreased feeding performance, and the fast open phase of the gape cycle became significantly longer, relative to the other phases. The tongue made similar shapes in both the control and nerve block conditions, but the pattern of tongue-jaw coordination became significantly more variable after the block. Disruption of oral somatosensation impacts feeding performance by introducing variability into the typically tight pattern of tongue-jaw coordination. During swallowing, tongue base retraction (TBR) drives the food bolus across the oropharynx towards the esophagus but the mechanics of TBR are poorly understood. XROMM of macaque monkeys falsifies both the hypothesis that extrinsic tongue muscle shortening pulls the tongue base posteriorly, and the muscular hydrostat hypothesis that intrinsic muscle shortening displaces the tongue base posteriorly. Our data suggest a novel hydraulic mechanism of TBR in which shortening and rotation of suprahyoid muscles compresses the tongue between the hard palate, hyoid and mouth floor, squeezing the midline tongue base and food bolus into the oropharynx. 

SEB Annual Conference 2022

3D Hyolingual Kinematics Reveal New Insights Into Biomechanical And Neural Control Of Chewing And Swallowing In Primates.

Discover the art of creating extraordinary science at SEB’s Annual Conference at Le Corum Conference Center     in Montpellier, France from 5 to  8 July 2022.

SEB’s Annual Conference is celebrated for creating the perfect composition of research, new discoveries and collaborative connections. Be creative and innovative by exchanging ideas and knowledge with masters of biology from all over the world.

2022 will find over 1500 experimental biologists from across the globe converging on the third-largest French city near the Mediterranean coast and the fastest-growing city in the country over the past 25 years.
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2022 will find over 1500 experimental biologists from across the globe converging on the third-largest French city near the Mediterranean coast and the fastest-growing city in the country over the past 25 years - Montpellier, France

technical paper

Kestrels exhibit steady flight in gusty conditions, including maintaining a headlock whilst soaring in strong winds; known as “windhovering”. Trying to understand what gives them this remarkable ability, and perhaps how this could be utilised in the growing area of drone flight is not feasible outdoors as it would require simultaneous measurements of the impinging atmospheric wind and wing, body and tail kinematics. We describe a novel wind-tunnel facility which enables such studies; whereby an updraft provides the environment to continuously soar, and upstream turbulence grids can generate a range of smooth and turbulent flows. To provide discrete gusts we have also developed a dedicated gust generator where prior calibration gives us time-accurate knowledge of a range of gust profiles. In a range of smooth and turbulent conditions the kinematics of two Nankeen Kestrels were documented using multiple cameras tracking reflective markers fixed to their wings, tails and bodies. Initial results have demonstrated the feasibility of the facility and techniques and have shown insights into the coupling between wing body and tail kinematics. An unexpected finding is that both birds favoured yawed flight (~30 degrees to the mean wind direction) which is potentially due to localising targets in their visual fovea.

Studying Kestrels Soaring in a Wind Tunnel: The Facility, Techniques and Initial Results

Birds’ wings have a high number of potentially independent degrees of freedom of motion. This enables their wings to morph in shape to suit a range of flight conditions, but potentially increases the complexity of flight control. Here we used motion tracking data from Nankeen kestrels (Falco cenchroides) performing steady wind hovering flights in a wind tunnel to study how different degrees of freedom in wing motion changed as the birds held station. To judge the contribution of a particular degree-of-freedom to flight control, metrics such as variance, correlation and control effectiveness were considered, along with Principal Component Analysis. Wing sweep, which represents the flexion/extension movement of the wing, was the major component of almost all wing motions. This was followed by sectional twist at the root, which although showing lower actuation, would have a strong effect on aerodynamic loads. Together these results highlight the major wing motions which contribute to the wind hovering flight of kestrels and suggest degrees of freedom to concentrate on when considering the design of future agile morphing wing uncrewed air vehicles.

Wing biomechanic couplings of kestrels during wind hovering flight

Animals are frequently faced with the challenge of negotiating unfamiliar structured environments during goal-oriented behaviours. Recent work on visually-guided flight through clutter has conceptualised this as a process of identifying and negotiating gaps that are broadly aligned with the animal’s expected or intended goal. These gaps are thereby conceived as attractors in their own right, rather than as features incidental to obstacles acting as repellers. Here we ask what information birds use to detect and fly through such gaps by tracking pigeons flying through an artificial forest of vertical poles. We find evidence for pigeons combining brightness cues with the sizes of visual gaps available ahead to choose which clearances to fly through. Modelling the free-flight behaviour as a process of sequential gap selection allows us to decompose it into components that can be independently evaluated. We find the observed behaviour is best captured by an autoregressive model including the effect of brightness, the absolute distance between obstacles and apparent visual gaps between a bird’s position and the end of the obstacle field. This can, in turn, be combined with established models of pigeon steering to provide a more complete picture of how birds guide their flight through complex environments

Creating a path where there is none: strategies for guidance in cluttered environments

Geometric scaling predicts a major constraint for legged, terrestrial locomotion. Locomotor support requirements at dynamically equivalent speeds scale isometrically with body mass (α M1), while force generation capacity should scale α M2/3 as it depends on tissue cross-sectional area. Mammals compensate with more upright postures at larger sizes, but it remains unknown how sprawling tetrapods deal with this constraint. Varanid lizards are an ideal group to address this question because they cover an enormous body size range while maintaining similar posture and body proportions. This study reports the scaling of joint moments from the hindlimb and forelimb from varanid species ranging from 7-37,000 g. Joint moments were calculated via inverse kinematics and inverse dynamics in OpenSim using a Varanus varius model scaled to the size of each species.  Peak joint moments scale between M1-1.4 in both limbs. Joint moments associated with stance phase (e.g. hip adduction, knee flexion, and ankle plantarflexion) generally scale higher (~ α M1.35-1.45) than those associated with swing phase (e.g. knee extension, ankle dorsiflexion) (~ α M1.1-1.35 in the hindlimb. Muscle parameters (fascicle length, muscle mass, physiological cross-sectional area, and fibre cross-sectional area) were also found to scale with positive allometry in varanids, suggesting that varanid lizards respond to predicted biomechanical demands of increased body size with both anatomical and kinematic adjustments. These results provide insight into the scaling of sprawling locomotion generally, and biomechanics of extinct, sprawling megafauna.

Locomotor joint moments in monitor lizards (Varanidae) and the scaling of locomotion in sprawling tetrapods

Negotiating sloping branches is a crucial aspect of arboreal life as animals must efficiently ascend and descend various supports. Climbing vertical supports likely played a major role in the acquisition of unique early primate specializations, but the functional and evolutionary interpretations of their locomotor, grasping, and visual adaptations, and their dependence on the arboreal environment remain unclear. Moreover, very little is known about descents in mammals. We investigated postural, kinematic, and grasping characteristics during ascents and descents on vertical supports in 22 small arboreal mammals, including 11 strepsirrhine and platyrrihine primates, 1 scandentian, 3 rodents, 3 carnivorans and 4 marsupials. We linked these behaviors to key morphological parameters to help reconstruct the paleoecology of extinct euarchontoglires. Vertical descents induced specific locomotor adjustments compared to ascents, notably increasing the proportion of asymmetrical gaits in all animals surveyed. Also, while all non-primate species preferentially employed headfirst descents regardless of their morphologies and body mass, primates exhibited specific upright strategies with strepsirrhines descending rump-first and platyrrhines descending in a side posture. Surprisingly, these upright vertical descents of primates were quite efficient compared to other mammals, allowing them to maintain higher speed and grasping postural diversity. Arboreal postural adaptations are highly influenced by the evolutionary history of mammals and result from a trade-off between body mass, limb proportions, grasping abilities and head size. We propose an ecological scenario of the sequence of acquisition of early primate grasping and locomotor specializations, constituting a hitherto unrecognized prerequisite for the origin of their encephalization.

The upright posture hypothesis: vertical descents in small arboreal mammals sheds light on the origins of primate specializations

Mobula rays are large marine fishes that filter great volumes of water and zooplankton with 
minimal clogging using highly specialized filter structures. Previous studies on simplified manta 
filter structures revealed a unique solid-fluid separation mechanism, now known as ricochet 
separation. These studies provide a basic understanding of this novel mechanism, but used a 
generalized model that did not account for the intricacy and diversity of the filter structures 
observed in mobulas. To better understand both the biology of mobula and the fluid dynamic 
processes that govern ricochet separation, this study investigated how morphological variation 
among mobula filters changes the filtration mechanisms and filter performance. We used microCT scans to 3D print biologically accurate filter models in four species of mobula. We visualized 
flow across and through the filters using digital particle image velocimetry (DPIV). We found 
that the differences in filter lobe morphology affected flow pressure and velocity as water moved 
through the filter pore. This inevitably affects the particle selectivity of the filter. This work can 
be used to guide engineers in creating biomimetic systems that can effectively filter particles 
smaller than the pore size without suffering clogging effects.

Manta mouthfuls: modeling accurate mobula morphology for flow analysis

Male northern quolls (Dasyurus hallucatus) die after a single synchronous breeding season, while females live and breed for 2-3 years. This provides a unique life history strategy in which to explore sex differences in performance trade-offs. Here, we assessed whether sprinting and biting performance trade-off for male or female northern quolls before, during, or after breeding (2012-2014). The activities that define survival and reproductive success for all animals depend on movement. However, movement is a complex trait, affected by multiple underlying factors, and organisms must balance the competing demands of these factors whenever they move. The morphology that increases bite force in northern quolls (i.e., increased head size)—which can improve fighting ability—should constrain sprinting performance by adding mass to the body. Trade-offs between fighting and escape performance might therefore be sex-specific or manifest only during particular times, such as during breeding. We studied northern quolls in the wild, and found that bite force and sprint speed do not trade-off functionally — bigger, heavier quolls with greater bite forces are not slower sprinters. We also found that males sprint slower in the post-breeding season. Because we have high recapture rates, we also assessed the repeatability of performance traits across several temporal scales. Performance was highly repeatable within seasons, but less repeatable across seasons, likely associated with the costs of the species’ extreme breeding. These findings suggest that ecologically relevant tasks important for survival and reproduction—fighting capacity and locomotor performance—may evolve independently in male and female northern quolls.

Performance trade-offs in the world’s largest semelparous mammal, the Australian northern quoll (Dasyurus hallucatus)

Locomotion is essential for fitness as it facilitates predation, escape, and reproductive behaviours. The energy expended for a given distance travelled (cost of transport; COT) varies significantly between individuals of the same species. Lower COT allows animals to allocate more of their energy budget to growth and reproduction. High COT may cause animals to adjust their movements to reduce energy allocated to movement, and potentially reduce energy allocation trade-offs. Our aim was to determine whether COT is a repeatable trait within individuals, and to determine its physiological causes and ecological consequences. We found that COT is a repeatable trait in zebrafish (Danio rerio). We rejected the hypothesis that mitochondrial efficiency (P/O ratio) predicted COT. We also rejected the hypothesis that COT is sensitive to temperature acclimation, exercise training, or their interaction, although COT increased with increasing acute test temperature. There was a weak but significant negative correlation between COT and dispersal, measured as the number of exploration decisions made by fish, and the distance travelled against the current in an artificial stream. However, COT did not correlate with the realised speed of fish swimming against the current. The implications of these results are that COT is an inherent characteristic of an individual which reflects a fixed physiological phenotype. Consequently, different energy budgets may be associated with individual movement patterns across environments. Warming environments may increase COT and exacerbate the magnitude of difference between individuals.

Cost of transport is a repeatable trait but is not determined by mitochondrial efficiency in zebrafish (Danio rerio)

Rose chafer beetles (Protetia cuprea) are pollinators as well as agricultural pests, flying between flowers and trees while foraging for pollen and fruits. Calculating the energy they expend on flying during foraging activity faces the challenge of measuring the metabolic rate (MR) of free-flying insects in an open space. We overcame this challenge by using the bolus injection of 13C Na-bicarbonate technique to measure their metabolic energy expenditure while flying in a large flight arena. Concurrently, we tracked the insects with high-speed cameras to extract their flight trajectory, from which we calculated the mechanical power invested in flying for each flight bout. We found that the chemical (metabolic) energy input converted to mechanical flight energy output at a mean efficiency of 10.4 ± 5.2 %, with a trend of increased efficiency in larger conspecifics (efficiency scaled with body mass to the power of 1.4). The transition during summer from a diet of pollen to that of fruits may affect the energy budget available for foraging. Starved P. cuprea, feeding on apples ad libitum, increased their body mass by an average of 6% in two hours. According to our calculations such a meal can power a 630-meter flight (assuming a carbohydrate assimilation efficiency of 90%). The high cost of aerial locomotion is inherent to the foraging behaviour of rose chafers, explaining their short flight bouts followed by prolonged feeding activity. The ability to measure both flight and its energetic cost is crucial for obtaining realistic estimates for the cost of locomotion.

The metabolic cost of flight and aerobic efficiency in the rose chafer, Protaetia cuprea (Cetoniinae)

Wing morphing during flight expands the performance envelope of flying animals and likely facilitates their ability to adapt to a broad range of habitats and atmospheric conditions. In birds, wing morphing is achieved by coupling a series of flexible and passive individual feathers to active musculoskeletal components. Although the aerodynamic effects of wing shape are relatively well characterised, the changes to the mechanical properties due to the structural rearrangement of feathers and the effects these changes have on flight performance are unknown. We first used dynamic mechanical testing at the base of in situ feathers of pigeons (Columba livia) to characterise the local mechanical properties. Wing folding decreased feather-anchoring tissue stiffness, an effect overcome in the proximal wing by an increase in stiffness via feather-feather interaction. We next applied computational fluid-structural interaction methods to quantify the effect of increasing or decreasing wing stiffness in the context of wing shape. These data revealed that the trends in wing stiffness due to wing folding can enhance lift production. Specifically, folding prevented destructive interference by the aerostructural deformations on flow vortices during high speed gliding flight. In conclusion, this study proposes that the natural coupling in the avian wing structural system between passive flight feathers and active musculoskeletal actuators allows for aerostructural flow control for enhanced flight performance over a variety of flight speeds.

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3D Hyolingual Kinematics Reveal New Insights Into Biomechanical And Neural Control Of Chewing And Swallowing In Primates.

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