Collective movement of schooling fish reduces the costs of locomotion in turbulent conditions.

The ecological and evolutionary benefits of energy-saving in collective behaviors are rooted in the physical principles and physiological mechanisms underpinning animal locomotion. We propose a turbulence sheltering hypothesis that collective movements of fish schools in turbulent flow can reduce the total energetic cost of locomotion by shielding individuals from the perturbation of chaotic turbulent eddies. We test this hypothesis by quantifying energetics and kinematics in schools of giant danio (Devario aequipinnatus) and compared that to solitary individuals swimming under laminar and turbulent conditions over a wide speed range. We discovered that, when swimming at high speeds and high turbulence levels, fish schools reduced their total energy expenditure (TEE, both aerobic and anaerobic energy) by 63% to 79% compared to solitary fish (e.g., 228 versus 48 kj kg-1). Solitary individuals spend approximately 22% more kinematic effort (tail beat amplitude•frequency: 1.7 versus 1.4 BL s-1) to swim in turbulence at higher speeds than in laminar conditions. Fish schools swimming in turbulence reduced their three-dimensional group volume by 41% to 68% (at higher speeds, approximately 103 versus 33 cm3) and did not alter their kinematic effort compared to laminar conditions. This substantial energy saving highlights that schooling behaviors can mitigate turbulent disturbances by sheltering fish (within schools) from the eddies of sufficient kinetic energy that can disrupt locomotor gaits. Therefore, providing a more desirable internal hydrodynamic environment could be one of the ecological drivers underlying collective behaviors in a dense fluid environment.

The role of hydrodynamics in collective motions of fish schools and bioinspired underwater robots.

Collective behaviour defines the lives of many animal species on the Earth. Underwater swarms span several orders of magnitude in size, from coral larvae and krill to tunas and dolphins. Agent-based algorithms have modelled collective movements of animal groups by use of social forces, which approximate the behaviour of individual animals. But details of how swarming individuals interact with the fluid environment are often under-examined. How do fluid forces shape aquatic swarms? How do fish use their flow-sensing capabilities to coordinate with their schooling mates? We propose viewing underwater collective behaviour from the framework of fluid stigmergy, which considers both physical interactions and information transfer in fluid environments. Understanding the role of hydrodynamics in aquatic collectives requires multi-disciplinary efforts across fluid mechanics, biology and biomimetic robotics. To facilitate future collaborations, we synthesize key studies in these fields.

Directional takeoff, aerial righting, and adhesion landing of semiaquatic springtails.

Springtails (Collembola) have been traditionally portrayed as explosive jumpers with incipient directional takeoff and uncontrolled landing. However, for these collembolans that live near the water, such skills are crucial for evading a host of voracious aquatic and terrestrial predators. We discover that semiaquatic springtails, Isotomurus retardatus, can perform directional jumps, rapid aerial righting, and near-perfect landing on the water surface. They achieve these locomotive controls by adjusting their body attitude and impulse during takeoff, deforming their body in midair, and exploiting the hydrophilicity of their ventral tube, known as the collophore. Experiments and mathematical modeling indicate that directional-impulse control during takeoff is driven by the collophore's adhesion force, the body angle, and the stroke duration produced by their jumping organ, the furcula. In midair, springtails curve their bodies to form a U-shape pose, which leverages aerodynamic forces to right themselves in less than ~20 ms, the fastest ever measured in animals. A stable equilibrium is facilitated by the water adhered to the collophore. Aerial righting was confirmed by placing springtails in a vertical wind tunnel and through physical models. Due to these aerial responses, springtails land on their ventral side ~85% of the time while anchoring via the collophore on the water surface to avoid bouncing. We validated the springtail biophysical principles in a bioinspired jumping robot that reduces in-flight rotation and lands upright ~75% of the time. Thus, contrary to common belief, these wingless hexapods can jump, skydive, and land with outstanding control that can be fundamental for survival.

Fire ant rafts elongate under fluid flows.

Fire ants survive flash floods by linking their bodies together to build waterproof rafts. Most studies of fire ant rafts consider static water conditions, but here, we consider the influence of flow. In particular, when floating on shallow water, the raft can run aground on vegetation, generating stresses in the raft as the water continues to flow around it. In this combined experimental and numerical study, we film the 10 h response of a fire ant raft caught on an anchor and subjected to water flows of 6 cm s-1. In this situation, ant rafts elongate from circular to more streamlined shapes, doubling in aspect ratio before eventually contracting back into smaller circular shapes as they enter dormancy. Ants in upstream regions of the raft exhibit less exploration activity than those downstream, suggesting that ants migrate to areas of lower fluid stress. While the raft is rough, hydrophobic, and heterogeneous in height, we may gain some insight by performing both fluid-structure interaction and agent based simulations on smooth rafts. Elongation to the degree observed is associated with a 48% drag reduction. Moreover, a purely elastic raft does not elongate, but conversely increases its bluff body cross-sectional area. We conclude that ant raftsmust reconfigure to generate the elongated shape observed. This work may provide insights into designing intelligent robotic swarms that can adapt to fluid flows.

Metabolic scaling of fire ants (Solenopsis invicta) engaged in collective behaviors.

During flash floods, fire ants (Solenopsis invicta Buren) link their bodies together to build rafts to stay afloat, and towers to anchor onto floating vegetation. Can such challenging conditions facilitate synchronization and coordination, resulting in energy savings per capita? To understand how stress affects metabolic rate, we used constant-volume respirometry to measure the metabolism of fire ant workers. Group metabolic rates were measured in a series of conditions: at normal state, at three elevated temperatures, during rafting, and during tower-building. We hypothesized that the metabolic rate of ants at various temperatures would scale isometrically (proportionally with the group mass). Indeed, we found metabolic rates scaled isometrically under all temperature conditions, giving evidence that groups of ants differ from entire colonies, which scale allometrically. We then hypothesized that the metabolism of ants engaged in rafting and tower-building would scale allometrically. We found partial evidence for this hypothesis: ants rafting for short times had allometric metabolic rates, but this effect vanished after 30 min. Rafting for long times and tower-building both scaled isometrically. Tower-building consumed the same energy per capita as ants in their normal state. Rafting ants consumed almost 43% more energy than ants in their normal state, with smaller rafts consuming more energy per capita. Together, our results suggest that stressful conditions requiring coordination can influence metabolic demand. This article has an associated First Person interview with the first author of the paper.

Caenorhabditis elegans exhibits positive gravitaxis.

BACKGROUND: Gravity plays an important role in most life forms on Earth. Yet, a complete molecular understanding of sensing and responding to gravity is lacking. While there are anatomical differences among animals, there is a remarkable conservation across phylogeny at the molecular level. Caenorhabditis elegans is suitable for gene discovery approaches that may help identify molecular mechanisms of gravity sensing. It is unknown whether C. elegans can sense the direction of gravity. RESULTS: In aqueous solutions, motile C. elegans nematodes align their swimming direction with the gravity vector direction while immobile worms do not. The worms orient downward regardless of whether they are suspended in a solution less dense (downward sedimentation) or denser (upward sedimentation) than themselves. Gravitaxis is minimally affected by the animals' gait but requires sensory cilia and dopamine neurotransmission, as well as motility; it does not require genes that function in the body touch response. CONCLUSIONS: Gravitaxis is not mediated by passive forces such as non-uniform mass distribution or hydrodynamic effects. Rather, it is mediated by active neural processes that involve sensory cilia and dopamine. C. elegans provides a genetically tractable system to study molecular and neural mechanisms of gravity sensing.

Terrain following and applications: Caenorhabditis elegans swims along the floor using a bump and undulate strategy.

Nematodes such as Caenorhabditis elegans are heavier than water. When submerged in water, they settle to the bottom surface. Observations reveal that the animals do not lie flat on the bottom surface, but remain substantially suspended above the surface through continuous collisions with the surface, while maintaining their swimming gaits. Consequently, the swimming animals follow the bottom surface topography. When the bottom surface is inclined, the animals swim up or down along the incline. As the magnitude of the gravitational force can be easily estimated, this behaviour provides a convenient means to estimate the animal's propulsive thrust. The animals' tendency to follow the surface topography provides a means to control the swimmers' trajectories and direction of motion, which we demonstrate with a saw tooth-like ratchet that biases the animals to swim in a selected direction. The animals can also serve as surface topography probes since their residence time as a function of position provides information on surface features. Finally, we take advantage of surface following to construct a simple motility-based sorter that can sort animals based on genotype and state of health.