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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

SEB Annual Conference 2022

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

technical paper

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.

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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

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.

Mechanisms for aerostructural flow control during avian wing morphing

When flying in near ground environments, birds encounter obstacles that force deviations from their flight paths. This raises the question of how they achieve the necessary guidance and control to perform these manoeuvres safely. In a flight arena equipped with a motion capture system, we challenged four Harris' hawks to negotiate a horizontal bar along their flight path between two perches (14 m apart). The unobstructed trajectory of the birds consists of a powered dive followed by glide up to the landing perch. The horizontal bar was positioned halfway between the perches, and was actuated to go through a vertical composite sinusoidal motion. While the minimum height of the bar was such that the typical unobstructed trajectory would not lead to a collision, the perceived risk of collision caused approximately half of the 880 flights to divert over the bar. The likelihood of diverting was primarily affected by the height of the bar and variation in individual preference. In cases where they would pass over the bar, three individuals directed their flight paths towards the bar shortly after take-off. This tracking mechanism, which arises as a risk averse behaviour, guides the birds nearer to the obstacle and thus increases the risk of collision. Obstacles acting as attractors would explain how many birds collide with overhead lines, despite the marginal probability for a random trajectory to encounter them.

Obstacle negotiation in the vertical plane

To produce the aerodynamic forces required for flight, two-winged insects (Diptera) move their wings back and forth at high wingbeat frequencies. Because the angular accelerations of this oscillating wing system scales quadratically with the wing-beat frequency, acceleration-based forces as a result of wing stroke-accelerations are expected to be particularly high for these flying insects. These acceleration-based forces consist of added-mass forces and Wagner-effect-based forces. Added-mass forces are resulting from the acceleration of fluid around the wing, and the Wagner-effect describes the delay in bound circulation build-up in accelerating wings. Here, we used computational fluid dynamics (CFD) simulations to systematically study how both added-mass forces and the Wagner-effect affect aerodynamic force production and airflow dynamics in accelerating insect wings. Based on the simulation results, we developed an aerodynamic model that captures the stroke-acceleration forces based on the wing-beat kinematics and wing morphology. This shows that current added-mass models fail to accurately predict added-mass forces on insect wings, primarily because these semi-empirical models ignore the Wagner-effect. Our novel Wagner-effect model is based on the interaction between stroke-rate and stroke-acceleration, and accurately predicts the delay in Leading-Edge Vortex build-up in accelerating wings as well as the delay in Leading-Edge Vortex reduction in decelerating wings. Finally, we applied our newly-developed aerodynamic model in a quasi-steady approach to the wingbeats of a fruit fly and malaria mosquito. This shows that particularly for high-frequency flapping flyers such as the mosquito, acceleration-based forces contribute substantially to aerodynamic lift and drag production.

Added-mass and Wagner-effect-based forces in high-frequency flapping insect wings

Humans are efficient bipedal walker and runner. Extant non-human primates (NHP) are not habitual bipeds, yet, they occasionally walk bipedally. According to 2D kinematics, they use a typical &quot;bent-hip, bent-knee&quot; posture coupled with a forward-leaning trunk, a limited stride length, a high stride frequency, and knees that remain flexed during the stance phase. No structural specialization is required for them to occasionally walk bipedally and compared to humans, extant NHPs do not exhibit any adaptations for bipedalism. Hence, it is suggested that the origin of a more habitual form of bipedal locomotion emerged from the common pattern observed in NHPs. However, one wonders whether the general lens through which the bipedal gait in NHPs has been described is discriminating enough to identify subtle differences that might exist between species. We conducted a study on the bipedal walking of olive baboons, at the Primatology Station of the CNRS (UAR 846). We provide detailed information on the 3D kinematics of bipedal walking. Our results show that the common pattern of the joint and segment angles can be easily described in the sagittal plan, but specificities related to the baboon model can be described in the frontal plan, such as the adduction of the thigh at touch-down. We compare these results with the 3D kinematics available for chimpanzees, capuchins, macaques and gibbons and identify subtle differences between species. Fundings: IRN-GDRI0870 & HoBiS-ANR-18-CE27-0010-01

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