Odour motion sensing enhances navigation of complex plumes.

Odour plumes in the wild are spatially complex and rapidly fluctuating structures carried by turbulent airflows1-4. To successfully navigate plumes in search of food and mates, insects must extract and integrate multiple features of the odour signal, including odour identity5, intensity6 and timing6-12. Effective navigation requires balancing these multiple streams of olfactory information and integrating them with other sensory inputs, including mechanosensory and visual cues9,12,13. Studies dating back a century have indicated that, of these many sensory inputs, the wind provides the main directional cue in turbulent plumes, leading to the longstanding model of insect odour navigation as odour-elicited upwind motion6,8-12,14,15. Here we show that Drosophila melanogaster shape their navigational decisions using an additional directional cue-the direction of motion of odours-which they detect using temporal correlations in the odour signal between their two antennae. Using a high-resolution virtual-reality paradigm to deliver spatiotemporally complex fictive odours to freely walking flies, we demonstrate that such odour-direction sensing involves algorithms analogous to those in visual-direction sensing16. Combining simulations, theory and experiments, we show that odour motion contains valuable directional information that is absent from the airflow alone, and that both Drosophila and virtual agents are aided by that information in navigating naturalistic plumes. The generality of our findings suggests that odour-direction sensing may exist throughout the animal kingdom and could improve olfactory robot navigation in uncertain environments.

Boundary layer hydrodynamics of patchy biofilms.

Algal biofilms, ubiquitous in aquatic systems, reduce the performance of engineered systems and alter ecosystem processes. Biofilm morphology is dynamic throughout community development, with patchiness occurring due to periodic sloughing, but little is known about how community level physical structure affects hydrodynamics. This study uses high resolution particle image velocimetry (PIV) to examine spatially explicit turbulence over sparse, uniform and patchy biofilm at turbulent Reynolds numbers. All biofilms increase the near-bed turbulence production, Reynolds shear stress, and rotational flow compared to a smooth wall, and non-uniform biofilms have the greatest increase in these parameters, compared with a uniform or sparse biofilm. However, a higher drag coefficient over uniform biofilm compared with non-uniform biofilm indicates that percent coverage (the amount of area covered by the biofilm) is a useful predictor of a biofilm's relative effect on the total drag along surfaces, and in particular the effect on ship performance.

Roughness effects of diatomaceous slime fouling on turbulent boundary layer hydrodynamics.

Biofilm fouling significantly impacts ship performance. Here, the impact of biofilm on boundary layer structure at a ship-relevant, low Reynolds number was investigated. Boundary layer measurements were performed over slime-fouled plates using high resolution particle image velocimetry (PIV). The velocity profile over the biofilm showed a downward shift in the log-law region (ΔU+), resulting in an effective roughness height (ks) of 8.8 mm, significantly larger than the physical thickness of the biofilm (1.7 ± 0.5 mm) and generating more than three times as much frictional drag as the smooth-wall. The skin-friction coefficient, Cf, of the biofilm was 9.0 × 10-3 compared with 2.9 × 10-3 for the smooth wall. The biofilm also enhances turbulent kinetic energy (tke) and Reynolds shear stress, which are more heterogeneous in the streamwise direction than smooth-wall flows. This suggests that biofilms increase drag due to high levels of momentum transport, likely resulting from protruding streamers and surface compliance.

The energetic cost of filtration by demosponges and their behavioural response to ambient currents.

Sponges (Porifera) are abundant in most marine and freshwater ecosystems, and as suspension feeders they play a crucial role in filtering the water column. Their active pumping enables them to filter up to 900 times their body volume of water per hour, recycling nutrients and coupling a pelagic food supply with benthic communities. Despite the ecological importance of sponge filter feeding, little is known about how sponges control the water flow through their canal system or how much energy it costs to filter the water. Sponges have long been considered textbook examples of animals that use current-induced flow. We provide evidence that suggests that some species of demosponge do not use current-induced flow; rather, they respond behaviourally to increased ambient currents by reducing the volume of water filtered. Using a morphometric model of the canal system, we also show that filter feeding may be more energetically costly than previously thought. Measurements of volumetric flow rates and oxygen removal in five species of demosponge show that pumping rates are variable within and between species, with the more oxygen consumed the greater the volume filtered. Together, these data suggest that sponges have active control over the volume of water they process, which may be an adaptation to reduce the energetic cost of filtration in times of high stress.

Neurally Encoding Time for Olfactory Navigation.

Accurately encoding time is one of the fundamental challenges faced by the nervous system in mediating behavior. We recently reported that some animals have a specialized population of rhythmically active neurons in their olfactory organs with the potential to peripherally encode temporal information about odor encounters. If these neurons do indeed encode the timing of odor arrivals, it should be possible to demonstrate that this capacity has some functional significance. Here we show how this sensory input can profoundly influence an animal's ability to locate the source of odor cues in realistic turbulent environments-a common task faced by species that rely on olfactory cues for navigation. Using detailed data from a turbulent plume created in the laboratory, we reconstruct the spatiotemporal behavior of a real odor field. We use recurrence theory to show that information about position relative to the source of the odor plume is embedded in the timing between odor pulses. Then, using a parameterized computational model, we show how an animal can use populations of rhythmically active neurons to capture and encode this temporal information in real time, and use it to efficiently navigate to an odor source. Our results demonstrate that the capacity to accurately encode temporal information about sensory cues may be crucial for efficient olfactory navigation. More generally, our results suggest a mechanism for extracting and encoding temporal information from the sensory environment that could have broad utility for neural information processing.

Effects of antennule morphology and flicking kinematics on flow and odor sampling by the freshwater crayfish, Procambarus clarkii.

The flow structure around the lateral antennular flagellum of the freshwater crayfish, Procambarus clarkii, was quantified to determine how antennule morphology and flicking kinematics affect fine-scale flow surrounding their chemosensory sensilla, called aesthetascs. Particle image velocimetry was used to measure velocity and vorticity of flow between aesthetascs of dynamically scaled physical models of P. clarkii antennules. Results revealed that the spacing between aesthetascs and antennule flicking speed induces substantial changes in fluid flow near aesthetascs. The downstroke flicking motion of the antennule occurs at a peak speed of 2.7cm/s. The returnstroke occurs at approximately 70% of this speed, but the fluid velocity between aesthetascs during the returnstroke is approximately 15% compared with the downstroke. The significant decrease in fluid flow near aesthetascs results from the reduced antennule speed and from the coupled interaction of boundary layers of the aesthetascs and antennule during the returnstroke. Odorant-laden fluid captured during the downstroke is retained between the aesthetascs during the slower returnstroke, and sufficient time occurs for odorant molecules to molecularly diffuse to aesthetasc surfaces. In addition, locally generated vorticity was observed near the tip of the aesthetascs, which may induce odorant transport to aesthetasc surfaces and enhance olfactory response times to odors.

Simultaneous sampling of flow and odorants by crustaceans can aid searches within a turbulent plume.

Crustaceans such as crabs, lobsters and crayfish use dispersing odorant molecules to determine the location of predators, prey, potential mates and habitat. Odorant molecules diffuse in turbulent flows and are sensed by the olfactory organs of these animals, often using a flicking motion of their antennules. These antennules contain both chemosensory and mechanosensory sensilla, which enable them to detect both flow and odorants during a flick. To determine how simultaneous flow and odorant sampling can aid in search behavior, a 3-dimensional numerical model for the near-bed flow environment was created. A stream of odorant concentration was released into the flow creating a turbulent plume, and both temporally and spatially fluctuating velocity and odorant concentration were quantified. The plume characteristics show close resemblance to experimental measurements within a large laboratory flume. Results show that mean odorant concentration and it's intermittency, computed as dc/dt, increase towards the plume source, but the temporal and spatial rate of this increase is slow and suggests that long measurement times would be necessary to be useful for chemosensory guidance. Odorant fluxes measured transverse to the mean flow direction, quantified as the product of the instantaneous fluctuation in concentration and velocity, v'c', do show statistically distinct magnitude and directional information on either side of a plume centerline over integration times of <0.5 s. Aquatic animals typically have neural responses to odorant and velocity fields at rates between 50 and 500 ms, suggesting this simultaneous sampling of both flow and concentration in a turbulent plume can aid in source tracking on timescales relevant to aquatic animals.

Micro-scale fluid and odorant transport to antennules of the crayfish, Procambarus clarkii.

A numerical model was developed to determine advective-diffusive transport of odorant molecules to olfactory appendages of the crayfish, Procambarus clarkii. We tested the extent of molecule transport to the surfaces of aesthetasc sensilla during an antennule flick and the degree of odorant exchange during subsequent flicks. During the rapid downstroke of a flick, odorant molecules are advected between adjacent aesthetascs, while during the slower return stroke, these odorants are trapped between the sensilla and molecular diffusion occurs over a sufficient time period to transport odorants to aesthetasc surfaces. During subsequent flicks, up to 97.6% of these odorants are replaced with new odorant molecules. The concentration of molecules captured along aesthetasc surfaces was found to increase with increased gap spacing between aesthetascs, flick speed, and distance from the proximal end of the aesthetasc, but these changes in morphology and flicking kinematics reduce the animal's ability to take discrete samples of the odorant-laden fluid environment with each flick. Results suggest that antennule flicking allows discrete sampling of the time- and space-varying odorant signal, and high concentration odorant filaments can be distinguished from more diffuse, low concentration filaments through changes in both the timing and the encounter rate of odorant molecules to aesthetasc surfaces.

The spatial and temporal patterns of odors sampled by lobsters and crabs in a turbulent plume.

Odors are dispersed across aquatic habitats by turbulent water flow as filamentous, intermittent plumes. Many crustaceans sniff (take discrete samples of ambient water and the odors it carries) by flicking their olfactory antennules. We used planar laser-induced fluorescence to investigate how flicking antennules of different morphologies (long antennules of spiny lobsters, Panulirus argus; short antennules of blue crabs, Callinectes sapidus) sample fluctuating odor signals at different positions in a turbulent odor plume in a flume to determine whether the patterns of concentrations captured can provide information about an animal's position relative to the odor source. Lobster antennules intercept odors during a greater percentage of flicks and encounter higher peak concentrations than do crab antennules, but because crabs flick at higher frequency, the duration of odor-free gaps between encountered odor pulses is similar. For flicking antennules there were longer time gaps between odor encounters as the downstream distance to the odor source decreases, but shorter gaps along the plume centerline than near the edge. In contrast to the case for antennule flicking, almost all odor-free gaps were <500 ms at all positions in the plume if concentration was measured continuously at the same height as the antennules. Variance in concentration is lower and mean concentration is greater near the substratum, where leg chemosensors continuously sample the plume, than in the water where antennules sniff. Concentrations sampled by legs increase as an animal nears an odor source, but decrease for antennules. Both legs and antennules encounter higher concentrations near the centerline than at the edge of the plume.

A non-canonical, interferon-independent signaling activity of cGAMP triggers DNA damage response signaling.

Cyclic guanosine monophosphate-adenosine monophosphate (cGAMP), produced by cyclic GMP-AMP synthase (cGAS), stimulates the production of type I interferons (IFN). Here we show that cGAMP activates DNA damage response (DDR) signaling independently of its canonical IFN pathways. Loss of cGAS dampens DDR signaling induced by genotoxic insults. Mechanistically, cGAS activates DDR in a STING-TBK1-dependent manner, wherein TBK1 stimulates the autophosphorylation of the DDR kinase ATM, with the consequent activation of the CHK2-p53-p21 signal transduction pathway and the induction of G1 cell cycle arrest. Despite its stimulatory activity on ATM, cGAMP suppresses homology-directed repair (HDR) through the inhibition of polyADP-ribosylation (PARylation), in which cGAMP reduces cellular levels of NAD+; meanwhile, restoring NAD+ levels abrogates cGAMP-mediated suppression of PARylation and HDR. Finally, we show that cGAMP also activates DDR signaling in invertebrate species lacking IFN (Crassostrea virginica and Nematostella vectensis), suggesting that the genome surveillance mechanism of cGAS predates metazoan interferon-based immunity.

Odor tracking in aquatic organisms: the importance of temporal and spatial intermittency of the turbulent plume.

In aquatic and terrestrial environments, odorants are dispersed by currents that create concentration distributions that are spatially and temporally complex. Animals navigating in a plume must therefore rely upon intermittent, and time-varying information to find the source. Navigation has typically been studied as a spatial information problem, with the aim of movement towards higher mean concentrations. However, this spatial information alone, without information of the temporal dynamics of the plume, is insufficient to explain the accuracy and speed of many animals tracking odors. Recent studies have identified a subpopulation of olfactory receptor neurons (ORNs) that consist of intrinsically rhythmically active 'bursting' ORNs (bORNs) in the lobster, Panulirus argus. As a population, bORNs provide a neural mechanism dedicated to encoding the time between odor encounters. Using a numerical simulation of a large-scale plume, the lobster is used as a framework to construct a computer model to examine the utility of intermittency for orienting within a plume. Results show that plume intermittency is reliably detectable when sampling simulated odorants on the order of seconds, and provides the most information when animals search along the plume edge. Both the temporal and spatial variation in intermittency is predictably structured on scales relevant for a searching animal that encodes olfactory information utilizing bORNs, and therefore is suitable and useful as a navigational cue.

Tracking Odorant Plumes.

Chemical signals are primarily distributed throughout aquatic environments by processes that are affected by turbulence. Turbulence continually stirs and mixes chemical odorants into complex, filamentous structures that are sampled by organisms. These odorant signals are critical for survival and/or reproductive success of most aquatic animals, and the time varying spatial structure of velocity and concentration offers valuable guidance cues while navigating in a plume. Two separate techniques are described to simultaneously measure a turbulent odor plume on a scale relevant to the chemosensors and mechanosensors located along the antennules of aquatic organisms. The first, planar laser induced fluorescence (PLIF), is used to quantify odorant concentrations, while the second, particle image velocimetry (PIV), is used to measure turbulent fluid velocities.

The role of turbulent hydrodynamics and surface morphology on heat and mass transfer in corals.

Corals require efficient heat and mass transfer with the overlying water column to support key biological processes, such as nutrient uptake and mitigation of thermal stress. Transfer rates are primarily determined by flow conditions, coral morphology and the physics of the resulting fluid-structure interaction, yet the relationship among these parameters is poorly understood especially for wave-dominated coral habitats. To investigate the interactive effects of these factors on fluxes of heat and mass, we measure hydrodynamic characteristics in situ over three distinct surface morphologies of massive stony corals in a Panamanian reef. Additionally, we implement a numerical model of flow and thermal transport for both current and wave conditions past a natural coral surface, as well as past three simplified coral morphologies with varying ratios of surface roughness spacing-to-height. We find oscillatory flow enhances rates of heat and mass transfer by 1.2-2.0× compared with unidirectional flow. Additionally, increases in Reynolds number and in surface roughness ratio produce up to a 3.3× and a 2.0× enhancement, respectively. However, as waves begin to dominate the flow regime relative to unidirectional currents, the underlying physical mechanisms mediating transfer rates shift from predominantly turbulence-driven to greater control by inertial accelerations, resulting in larger heat and mass transfer for small surface roughness ratios. We show that for rough corals in wave-dominated flows, novel trade-off dynamics for heat and mass transfer exist between broadly spaced roughness that enhances turbulence production versus narrowly spaced roughness that produces greater surface area. These findings have important implications for differential survivorship during heat-induced coral bleaching, particularly as thermal stress events become increasingly common with global climate change.

Flexibility of crab chemosensory sensilla enables flicking antennules to sniff.

The first step in smelling is capture of odorant molecules from the surrounding fluid. We used lateral flagella of olfactory antennules of crabs Callinectes sapidus to study the physical process of odor capture by antennae bearing dense tufts of hair-like chemosensory sensilla (aesthetascs). Fluid flow around and through aesthetasc arrays on dynamically scaled models of lateral flagella of C. sapidus was measured by particle image velocimetry to determine how antennules sample the surrounding water when they flick. Models enabled separate evaluation of the effects of flicking speed, aesthetasc spacing, and antennule orientation. We found that crab antennules, like those of other malacostracan crustaceans, take a discrete water sample during each flick by having a rapid downstroke, during which water flows into the aesthetasc array, and a slow recovery stroke, when water is trapped in the array and odorants have time to diffuse to aesthetascs. However, unlike antennules of crustaceans with sparse aesthetasc arrays, crabs enhance sniffing via additional mechanisms: 1) Aesthetascs are flexible and splay as a result of the hydrodynamic drag during downstrokes, then clump together during return strokes; and 2) antennules flick with aesthetascs on the upstream side of the stalk during downstrokes, but are hidden downstream during return strokes. Aiming aesthetascs into ambient flow maintains sniffing. When gaps between aesthetascs are wide, changes in antennule speed are more effective at altering flow through the array than when gaps are narrow. Nonetheless, if crabs had fixed gap widths, their ability to take discrete samples of their odorant environment would be diminished.

Effects of sensilla morphology on mechanosensory sensitivity in the crayfish.

Crustaceans contain a great variety of sensilla along their antennules that enable them to sense both hydrodynamic and chemical stimuli in aquatic environments, and can be used to inspire the design of engineered sensing systems. For example, along the antennule of the freshwater crayfish, Procambarus clarkii, four predominant mechanosensory sensilla morphologies are found. To study their response to upstream flow perturbations, atomic force microscopy was utilized to determine P. clarkii sensilla bending in response to an applied force and a mean torsional stiffness, k(t) = 1 × 10(-12) N m degree(-1) was found. A numerical model was developed to quantify the deformation of the four sensilla morphologies due to flow perturbations within their surrounding fluid. These flow perturbations were intended to mimic predator and ambient fluid movements. Results show that upstream fluid motion causes alterations in velocity near the sensilla, accompanied by corresponding variations in pressure along the sensilla surface. The feathered and filamentous sensilla, which are hydrodynamic sensilla, were found to be highly sensitive to flow perturbations. The beaked and asymmetric sensilla, which are bimodal chemo-mechanoreceptors, were found to be much less sensitive to hydrodynamic disturbances. Results also show that sensilla are most sensitive to fluid movement in the along-axis plane of the antennule, with a sharp drop in sensitivity perpendicular to this axis. This sensitivity agrees well with neural responses measured directly from the paired sensory neurons associated with each sensillum. Greater along-axis sensitivity is likely beneficial for determining the direction of fluid movements, which may be important for both aquatic organisms and biomimetic sensing systems.

A nose too far: regional differences in olfactory receptor neuron efficacy along the crayfish antennule.

The olfactory sense organs of crayfish are aesthetasc sensilla, arrayed along the distal half of the lateral antennular flagella on each side of the animal. The sensillar array is sparse at its proximal origin, where each annulus houses only a single aesthetasc, and it is most dense distally, with occasionally up to six aesthetascs residing on each antennular annulus. Previous studies have tacitly assumed that the aesthetascs are co-equal in their functional properties. We restricted exposure of small zones of aesthetascs to odorant along the array, from near its proximal origin, its midpoint, and its termination near the tip of the lateral flagellum, while recording neural responses within the ipsilateral olfactory lobe of the brain. Simultaneous combinations of zonal exposure to odorant gave proportionally larger central responses, indicative of spatial summation of peripheral inputs. Surprisingly, however, zonal effectiveness was not equal; stimulating even small numbers of aesthetascs near the proximal origin of the array was far more excitatory to local deutocerebral interneurons than stimulating greater numbers of aesthetascs at the tip of the flagellum. The results are discussed in terms of continuing growth and attrition of the antennular segmentation and associated olfactory receptor neurons.

Biophysical constraints on optimal patch lengths for settlement of a reef-building bivalve.

Reef-building species form discrete patches atop soft sediments, and reef restoration often involves depositing solid material as a substrate for larval settlement and growth. There have been few theoretical efforts to optimize the physical characteristics of a restored reef patch to achieve high recruitment rates. The delivery of competent larvae to a reef patch is influenced by larval behavior and by physical habitat characteristics such as substrate roughness, patch length, current speed, and water depth. We used a spatial model, the "hitting-distance" model, to identify habitat characteristics that will jointly maximize both the settlement probability and the density of recruits on an oyster reef (Crassostrea virginica). Modeled larval behaviors were based on laboratory observations and included turbulence-induced diving, turbulence-induced passive sinking, and neutral buoyancy. Profiles of currents and turbulence were based on velocity profiles measured in coastal Virginia over four different substrates: natural oyster reefs, mud, and deposited oyster and whelk shell. Settlement probabilities were higher on larger patches, whereas average settler densities were higher on smaller patches. Larvae settled most successfully and had the smallest optimal patch length when diving over rough substrates in shallow water. Water depth was the greatest source of variability, followed by larval behavior, substrate roughness, and tidal current speed. This result suggests that the best way to maximize settlement on restored reefs is to construct patches of optimal length for the water depth, whereas substrate type is less important than expected. Although physical patch characteristics are easy to measure, uncertainty about larval behavior remains an obstacle for predicting settlement patterns. The mechanistic approach presented here could be combined with a spatially explicit metapopulation model to optimize the arrangement of reef patches in an estuary or region for greater sustainability of restored habitats.

The sponge pump: the role of current induced flow in the design of the sponge body plan.

Sponges are suspension feeders that use flagellated collar-cells (choanocytes) to actively filter a volume of water equivalent to many times their body volume each hour. Flow through sponges is thought to be enhanced by ambient current, which induces a pressure gradient across the sponge wall, but the underlying mechanism is still unknown. Studies of sponge filtration have estimated the energetic cost of pumping to be <1% of its total metabolism implying there is little adaptive value to reducing the cost of pumping by using "passive" flow induced by the ambient current. We quantified the pumping activity and respiration of the glass sponge Aphrocallistes vastus at a 150 m deep reef in situ and in a flow flume; we also modeled the glass sponge filtration system from measurements of the aquiferous system. Excurrent flow from the sponge osculum measured in situ and in the flume were positively correlated (r>0.75) with the ambient current velocity. During short bursts of high ambient current the sponges filtered two-thirds of the total volume of water they processed daily. Our model indicates that the head loss across the sponge collar filter is 10 times higher than previously estimated. The difference is due to the resistance created by a fine protein mesh that lines the collar, which demosponges also have, but was so far overlooked. Applying our model to the in situ measurements indicates that even modest pumping rates require an energetic expenditure of at least 28% of the total in situ respiration. We suggest that due to the high cost of pumping, current-induced flow is highly beneficial but may occur only in thin walled sponges living in high flow environments. Our results call for a new look at the mechanisms underlying current-induced flow and for reevaluation of the cost of biological pumping and its evolutionary role, especially in sponges.

To paddle or not: context dependent courtship display by male blue crabs, Callinectes sapidus.

The nature of the courtship signalling used by a species is shaped by many factors, one of which is its habitat. Male blue crabs, Callinectes sapidus, have a courtship display in which they elevate their body by standing high on their legs, open their chelae and paddle their swimming legs. This courtship display is not reported in other swimming (portunid) crabs and is rarely expressed in laboratory experiments on male blue crabs. In this study, we characterised this display, which we call ;courtship stationary paddling', and distinguished it from other types of paddling. To explain the species specificity of courtship stationary paddling, we hypothesised that this behaviour is an adaptation to low visibility and abundant refuges in the habitat of blue crabs, and that this behaviour enhances chemical signalling when females are relatively inaccessible to males. We used particle imaging velocimetry to visualise water currents generated during courtship stationary paddling, showing that it created water currents directed away from the male and towards the female, thus enhancing chemical signalling. We also showed that males did not perform courtship stationary paddling when females were freely walking such that males could quickly contact and cradle carry them. Rather, males typically performed courtship stationary paddling only when females were inaccessible to them. These results indicate that courtship stationary paddling is a context-dependent behaviour, occurring only when females are not accessible to males, and suggesting that it evolved as an adaptation to life in habitats with many refuges and low visibility.