Assessing the state of biologically inspired design from three perspectives: academic, public, and practitioners.

Biologically inspired design (BID) applies natural solutions to engineering challenges. Due to the widespread success of BID, we examine the following research question: how does the purpose of applying, the inspiration source, and the application of BID differ between academics, the public, and practitioners? Answering this question can help us design the tools used to support BID, provide an understanding of the current 'state of BID' and identify where BID solutions have not been widely utilized. Identifying gaps in utilization could prompt investigations into BID methods in new fields. To answer this research question, 660 BID samples were gathered equally from three data sources: Google Scholar, Google News, and the Asknature.org 'Innovations' database. The data were classified across seven dimensions and 68 subcategories. The conclusions of our research deliver insights into three areas. First, we identify trends in BID independent of source. For example, 72.5% of the biomimicry samples had the purpose of improving functionality and 87.6% of the samples impacted the usage phase of a product's life cycle. Secondly, by examining the distribution of BID within each source, we identify areas for potential outreach or application. Finally, by contrasting BID results between three sources (academic, news, and practical case studies) we gain an understanding of the disparities between the three. This analysis provides BID researchers and practitioners with a useful insight into the present state of this field, with the goal of motivating future research and application.

Bioinspired algorithm for autonomous sensor-driven guidance in turbulent chemical plumes.

We designed and implemented a control algorithm for sensor-mediated chemical plume tracking in a turbulent flow environment. In our design, we focused on development of a signal processing strategy capable of replicating behavioral responses of actively tracking blue crabs (Callinectes sapidus) to chemical stimuli. The control algorithm is evaluated in a hardware platform that allows motion in two directions (i.e. forward-back and left-right). The geometric arrangement of the sensor array is inspired by the location of blue crab sensor populations. Upstream motion is induced by a binary response to supra-threshold spikes of concentration, and cross-stream steering is controlled by contrast between bilaterally-separated sensors. Like animal strategies, the developed control algorithm is dynamic. This property allows the algorithm to function effectively in the highly irregular turbulent environment and produces adaptive adjustments of motion to minimize the distance to the source of a plume. Tracking trials indicate that roughly 80% of the tracks successfully stop near the plume source location. Both success rate and movement patterns of the tracker compare favorably to that of blue crabs searching for odorant plume sources, thus suggesting that our sensory-mediated behavior hypothesis are generally accurate and that the associated tracking mechanisms may be successfully implemented in hardware.

Chemoreception in the salmon louse Lepeophtheirus salmonis: an electrophysiology approach.

The search for effective and long-term solutions to the problems caused by salmon lice Lepeophtheirus salmonis (Krøyer, 1837) has increasingly included biological/ecological mechanisms to combat infestation. One aspect of this work focuses on the host-associated stimuli that parasites use to locate and discriminate a compatible host. In this study we used electrophysiological recordings made directly from the antennule of adult lice to investigate the chemosensitivity of L. salmonis to putative chemical attractants from fish flesh, prepared by soaking whole fish tissue in seawater. There was a clear physiological response to whole fish extract (WFX) with threshold sensitivity at a dilution of 10 . When WFX was size fractionated, L. salmonis showed the greatest responses to the water-soluble fractions containing compounds between 1 and 10 kDa. The results suggest that the low molecular weight, water-soluble compounds found in salmon flesh may be important in salmon lice host choice.

Fluid mechanics produces conflicting, constraints during olfactory navigation of blue crabs, Callinectes sapidus.

Foraging blue crabs must respond to fluid forces imposed on their body while acquiring useful chemical signals from turbulent odor plumes. This study examines how blue crabs manage these simultaneous demands. The drag force, and hence the cost of locomotion, experienced by blue crabs is shown to be a function of the body orientation angle relative to the flow. Rather than adopting a fixed orientation that minimizes the drag, blue crabs decrease their relative angle (increase drag) when odor is present in low speed flow, while assuming a drag-minimizing posture under other conditions. The motivation for crabs to adopt an orientation with larger drag appears to relate to their ability to acquire chemical signal information for odor tracking. In particular, when orienting at a smaller angle relative to the flow direction, more concentrated odor filaments arrive at the antennules to mediate upstream movement, allowing a more useful bilateral comparison between the appendage chemosensors to be made. Blue crabs respond to conflicting demands by weighting the degree of drag minimization in proportion to the potential magnitude of the drag cost and the potential benefit of acquiring chemosensory cues. Higher flow velocity magnifies the locomotory cost of a high drag posture, thus in swift flows crabs minimize drag and sacrifice their ability to acquire olfactory cues.

Transsexual limb transplants in fiddler crabs and expression of novel sensory capabilities.

We used transsexual limb transplants in fiddler crabs to examine how peripheral sensory structures interact with the central nervous system (CNS) to produce a sexually dimorphic behavior. Female and male chemosensory feeding claws were transplanted onto male hosts in place of nonfeeding, nonchemosensory claws. Successfully transplanted claws retain donor morphologies and contain chemosensory neurons. Neurons in successfully transplanted female feeding claws express the enhanced sensitivity to chemical cues seen in female, but not male, neurons in claws of normal animals. When chemically stimulated, the transplanted claws evoke feeding behavior not observed in normal males, even though the sensory neurons in the transplanted limb project to the host's sexually dimorphic neuropil not known to receive chemosensory input. Behavioral sensitivity is directly related to the sensitivity of peripheral neurons in the transplanted feeding claw. Thus, the interactions between peripheral neurons and their targets may restructure the CNS so that novel sensory capabilities are expressed, and this can produce sexually dimorphic behaviors.

Sex, sensitivity, and second messengers: differential effect of cyclic nucleotide mediated inhibition in the chemosensory system of fiddler crabs.

Fiddler crabs (Uca spp.) exhibit sex-specific responses food-related chemical cues, constituting a natural experiment regarding the regulation of chemosensitivity. To understand the mechanisms that underlie these broad differences, chemosensory neurons from the claws were challenged with stimulants in the presence of various agents that activate or inhibit the adenylate cyclase-cAMP transduction cascade. Stimulants mixed with agents that increase intracellular cAMP (forskolin, 3-isobutyl-1-methylxanthine, and Ro 20-1724) elicited decreased response magnitudes from neurons, compared to drug-free controls, whereas the adenylate cyclase inhibitor SQ 22536 increased the response. These effects were dose dependent and reversible, and, in all cases, were more dramatic in male than in female neurons. Similar to other crustaceans, the adenylate cyclase-cAMP second-messenger system appears to regulate inhibition in fiddler crab chemosensory neurons. The perturbations of this pathway reveal that the degree of inhibition is greater in male than in female neurons, consistent with the lower behavioral and physiological sensitivity typically displayed by males. Changes in the expression of the second messenger system may be causal in the production of sex-specific patterns of chemosensitivity that underlie behavior. Alternately, experimental perturbations using adenylate cyclase-cAMP pathway modulators may unmask sex-specific differences in electrical properties of peripheral neurons affecting action potential generation.

The effects of fluid motion on toxicant sensitivity of the rotifer Brachionus calyciflorus.

Standardized methods for estimating the toxicity of anthropogenic compounds to aquatic organisms frequently fail to consider key elements of the test organisms' environment. Aquatic organisms exist in a fluid environment, and fluid dynamics may have an important influence on the response to toxicants. Rotifers are one of the three major groups of zooplankton and have been increasingly utilized in standardized toxicity testing. However, like other toxicity tests, assays with the species Brachionus calyciflorus are performed under static conditions in the absence of fluid motion. We investigated how fluid motion modifies pentachlorophenol (PCP) toxicity to B. calyciflorus using 24 h acute and 48 h reproductive toxicity tests. Estimates of PCP LC50s and reproduction EC50s in static conditions decreased from 738 and 1082 microg l(-1), respectively, to as low as 262 and 136 microg l(-1), respectively, in fluid motion. Flow analysis indicated that increased toxicant sensitivity can occur at ecologically relevant levels of fluid motion. Mechanistic studies indicated that fluid motion/toxicant interactions may result from the ability of fluid motion to cause shear stress, alter toxicant uptake, and/or alter the bioavailability of food. As fluid motion may have an important effect on the life histories of a wide variety of aquatic organisms, fluid motion/toxicant interactions may be an important consideration in other standard test organisms. These results raise questions about the accuracy of ecological risk assessments based on toxicity data from static conditions.

The fluid dynamical context of chemosensory behavior.

The fluid mechanical environment provides the context in which denizens of aquatic realms, as well as terrestrial creatures, use chemoperception to search for objects. Our ability to understand the nature of olfactory-guided navigation rests on our proficiency at characterizing the fluid dynamic setting and at relating properties of flow to behavioral and sensory mechanisms. This work reviews some fluid dynamical concepts that are particularly useful in describing aspects of flow relevant to chemosensory navigation, and it considers studies of orientation in animals in light of these principles. Comparisons across broadly different fluid environments suggest that particular sensory and behavioral mechanisms may be tailored to specific flow regimes and stimulus environments. This is clearly evident when examining animals that operate in high vs. low Reynolds number flows. In other cases, animals may converge on common solutions in given flow regimes in spite of differences in taxonomic class or size. Potential parallels may include behavior of aquatic vs. terrestrial arthropods, and animals without fixed reference points in flows dominated by molecular vs. turbulent diffusion. In an effort to add further fluid dynamical underpinnings to navigational strategies, I suggest how simple nondimensional categorization of behavior in relation to flow may aid in identifying the forces underlying common elements, even across animals of seemingly disparate size and scale.

Tuning breadth and sex-specific sensitivity in chemosensory neurons of male and female Uca pugnax.

Chemosensory neurons of female fiddler crabs (genus Uca) display greater sensitivity to mixtures of food-related stimuli than do neurons in males. This phenomenon represents an interesting contrast to other sex-specific systems, which tend to be in response to cues associated with mating and parental care. This study examined the responses of chemosensory neurons in males and females to ten individual stimuli to determine if sex-specific responses were restricted to a few key compounds, or if the heightened sensitivity of females was broadly distributed. Neurons in males and females responded well to all stimuli, and although fiddler crabs are primarily herbivorous, highly efficacious physiological stimulants included amino acids and amines as well as carbohydrates most closely associated with plant material. The chemosensory neurons are characterized by broad tuning and relatively high response thresholds, when compared to other crustaceans. Most importantly, the investigations revealed a robust pattern in which female neurons displayed elevated responses to all stimuli. Tuning breadth was not shown to be sex-specific, nor were there detectable differences in over-all response profiles. The most likely explanation for these patterns is that the broad sex-specificity in Uca is produced via fundamental alterations in cellular properties associated with chemosensory transduction.

Following the invisible trail: kinematic analysis of mate-tracking in the copepod Temora longicornis.

We have analysed the fine-scale kinematics of movement of male and female copepods, Temora longicornis, to resolve how these small animals find their mates. Location of the trail initially involves rapid random turning and high rates of directional change. Males subsequently increase their rate of movement as they follow the trail, and execute a regular pattern of counter turns in both x,z and y,z planes to stay near or within the central axis of the odour field. Pursuit behaviour of males is strongly associated with female swimming behaviour, suggesting that quantifiable variations in the structure of the odour signal released by females affects male tracking. The behavioural components of mate tracking in Temora are very similar to those of other animals that employ chemically mediated orientation in their search for mates and food, and we conclude that male Temora find their mates using chemoperception. The kinematic analysis indicates both sequential and simultaneous taxis mechanisms are used by Temora to follow the odour signal. This, in turn, indicates that rather than responding to a diffuse plume, males are following a signal more accurately characterized as a chemical trail, and copepods appear to use mechanisms that are similar to those employed by trail-following terrestrial insects such as ants. While Temora expresses similar behaviours to those of a variety of chemosensory organisms, the ability to track a three-dimensional odour trail appears unique, and possibly depends on the persistence of fluid-borne odour signals created in low Reynolds number hydrodynamic regimes.

The fluid physics of signal perception by mate-tracking copepods.

Within laboratory-induced swarms of the marine copepod Temora longicornis, the male exhibits chemically mediated trail-following behaviour, concluding with fluid mechanical provocation of the mate-capture response. The location and structure of the invisible trail were determined by examining the specific behaviour of the female copepods creating the signal, the response of the male to her signal, and the fluid physics of signal persistence. Using the distance of the mate-tracking male from the ageing trail of the female, we estimated that the molecular diffusion coefficient of the putative pheromonal stimulant was 2.7 x 10(-5) cm2 s-1, or 1000 times slower than the diffusion of momentum. Estimates of signal strength levels, using calculations of diffusive properties of odour trails and attenuation rates of fluid mechanical signals, were compared to the physiological and behavioural threshold detection levels. Males find trails because of strong across-plume chemical gradients; males sometimes go the wrong way because of weak along-plume gradients; males lose the trail when the female hops because of signal dilution; and mate-capture behaviour is elicited by suprathreshold flow signals. The male is stimulated by the female odour to accelerate along the trail to catch up with her, and the boundary layer separating the signal from the chemosensitive receptors along the copepod antennule thins. Diffusion times, and hence reaction times, shorten and behavioural orientation responses can proceed more quickly. While 'perceptive' distance to the odour signal in the trail or the fluid mechanical signal from the female remains within 1-2 body lengths (< 5 mm), the 'reactive' distance between males and females was an order of magnitude larger. Therefore, when nearest-neighbour distances are 5 cm or less, as in swarms of 10(4) copepods m-3, mating events are facilitated. The strong similarity in the structure of mating trails and vortex tubes (isotropic, millimetre-centimetre scale, 10:1 aspect ratio, 10s persistence), indicates that these trails are constrained by the same physical forces that influence water motion in a low Reynolds number fluid regime, where viscosity limits forces to the molecular scale. The exploratory reaches of mating trails appear inscribed within Kolmogorov eddies and may represent a measure of eddy size. Biologically formed mating trails, however, are distinct in their flow velocity and chemical composition from common small-scale turbulent features; and mechanoreceptive and chemoreceptive copepods use their senses to discriminate these differences. Zooplankton are not aimless wanderers in a featureless environment. Their ambit is replete with clues that guide them in their efforts for survival in the ocean.

Chemo- and mechanosensory orientation by crustaceans in laminar and turbulent flows: from odor trails to vortex streets.

Crustaceans use odor and fluid mechanical cues to extract information from their environment. These cues enable animals to find resources, orient to water currents, or escape predators. Because the properties of the fluid environment affect the transmission and structure of relevant signals, a better understanding of sensory and behavioral mechanisms will be aided by considering, at the same time, the hydrodynamic context of chemo- and mechanosensory behaviors. Crustaceans occupy aquatic habitats where flows range from almost completely laminar to nearly fully turbulent. The considerable scope of hydrodynamic properties is mirrored by equally extreme variations in the complexity of the signals entrained in these flows. Ambient noise and stochastic variation increase in increasingly energetic, turbulent conditions. The sensory and behavioral mechanisms of animals that orient in turbulent environments suggest that they have, in the course of evolution, been shaped by the flow properties. Here, sensory systems are geared to extract rapidly fluctuating signals against a noisy background. They sometimes have elaborate noise filtering mechanisms that enable the detection of rather coarse types of signal features to improve the signal-to-noise ratio. In contrast, the simpler and more predictable structure of signals carried in laminar flows may allow more accurate orientation and discrimination to occur, and free animals from the burden of supporting complex noise-filtering circuitry. Future comparative investigations of sensory physiology and behavior of animals in relation to their flow environment promise to increase our understanding of orientation by means of chemo- and mechanoperception.

Sexually dimorphic patterns of neural organization in the feeding appendages of fiddler crabs.

The organization of sensory nerves and sensilla was examined in the feeding claw of two species of fiddler crabs, Uca pugnax and U. pugilator, using neuroanatomical and behavioral techniques. Surveys of the populations of axons indicate that claws of adult crabs contain 25000-40000 neurons. Approximately 85% of the population consists of axons with diameters less than 1 microm, suggesting they may represent chemosensory neurons. Females show an enhanced population of these small (putative chemosensory) axons relative to males, providing a mechanism to explain previously observed sexual differences in behavioral chemosensitivity to feeding stimulants. Surveys of the claw surface show a variety of external structures that could contain either chemo- or mechanosensory receptor neurons. There are hair-like sensilla of several types, some of which are more abundant in females than in males. In addition, claws show previously undescribed pit sensilla reminiscent of known bimodal chemo- and mechanosensory sensilla found in certain decapod crustaceans. Morphological properties of hair-like sensilla, as well as their small number in relation to the large population of presumptive chemosensory axons, suggest that they have a limited role in chemosensation. Most of the chemosensory axons probably originate in the pit sensilla.

Regulation of sex-specific feeding behavior in fiddler crabs: physiological properties of chemoreceptor neurons in claws and legs of males and females.

This study examined properties of chemoreceptor neurons in the claws and legs of the fiddler crabs Uca pugilator and U. pugnax. The primary goal was to establish the neural basis of previously observed greater female sensitivity to feeding stimulants, and secondarily to compare physiological properties of chemoreceptor neurons in these semi-terrestrial crustaceans with those of fully aquatic forms. Sensitivity of chemoreceptor neurons in claws and legs is sex-specific; individual neurons of females respond to lower stimulus concentrations than male chemoreceptor neurons, and equivalent concentrations elicit greater spiking in female vs male chemoreceptor neurons. Thus, the population of chemoreceptor neurons in females expresses lower thresholds and greater average sensitivity than in males. Greater sensitivity of claw neurons explains observations indicating that females continue to feed at food levels too low to stimulate males. Sensitivity differences in leg neurons of males vs females have no clear behavioral correlate, but suggest that females can orient to more dilute stimuli than males. Chemoreceptor neurons of fiddler crabs have low sensitivities and slow rates of adaptation compared to other crustaceans. Also, neurons in claws adapt less slowly than neurons in legs, which may reflect subtle differences in the chemical stimulus environment experienced by claws vs legs.

Odor plumes and how blue crabs use them in finding prey.

Orientation of animals using chemical cues often takes place in flows, where the stimulus properties of odorants are affected by the characteristics of fluid motion. Kinematic analysis of movement patterns by animals responding to odor plumes has been used to provide insight into the behavioral and physiological aspects of olfactory-mediated orientation, particularly in terrestrial insects. We have used this approach in analyzing predatory searching by blue crabs in response to plumes of attractant metabolites released from the siphons of live clams in controlled hydrodynamic environments. Crabs proceed directly upstream towards clams in smooth-turbulent flows and show high locomotory velocities and few periods of motionlessness. Crabs assume more indirect trajectories and display slower locomotion and more stopping in rough-turbulent flows. This degradation of foraging performance is most pronounced as flow shifts from a smooth- to a rough-turbulent regime, where the change in hydraulic properties is associated with contraction of the viscous sublayer region of the boundary layer. Because flow in this region is quasilaminar, the viscous sublayer may be a particularly effective vehicle for chemical stimulus transmission, such that orientation is severely compromised when it is reduced or removed. Our results also suggest that rheotactic and chemical information are both necessary for successful orientation. Perception of chemical cues acts to bias locomotion upcurrent, and feedback from odorant stimulus distributions appears directly to regulate subsequent stopping and turning en route to prey. Although the mechanisms of orientation to odorant plumes displayed by insects and blue crabs are largely similar, blue crabs appear to rely more heavily on spatial and/or temporal aspects of chemical stimulus distributions than has been suggested for insect systems.

Spatial distribution of odors in simulated benthic boundary layer flows.

Many animals orient to odor sources in aquatic habitats where different flows and substrates affect the hydrodynamics of benthic boundary layers. Since the dispersal of chemicals is due to the fluid mechanics of a particular environment, we quantified the changes in the fine structure of an odor plume under different hydrodynamic conditions in the benthic boundary layer of a laboratory flume. We sampled turbulent odor plumes at 10 Hz using a microchemical sensor (150 µm diameter) under two flow speeds: 3.8 and 14.4 cm/sec, and at 1, 8, 50 mm above the substrate. These distances above the substrate occur within different flow regions of the boundary layer and correlate with the location of crustacean chemosensory appendages within boundary layer flows. The high flow velocity exhibited a greater level of turbulence and had more discrete odor pulses than the low flow velocity. In general, odor signals showed a high level of temporal variation in fast flow at heights 1 and 8 mm above the substrate. In slow flow, temporal variation was maximal at 50 mm above the substrate, exhibiting more variance than the same height at the fast flow. These patterns of odor signals resulted in part from differences in the height above the substrate of the main axis of the odor plume at the two flow speeds. Our results imply that animals chemically orienting to an odor source will need to compensate for varying hydrodynamic properties of odor transport and dispersal. The method by which animals extract spatial information from odor plumes will need to account for changing flow conditions, or else it will not be equally efficient in extracting information about chemical spatial distributions.

Measurement of Microscale Patchiness in a Turbulent Aquatic Odor Plume Using a Semiconductor-Based Microprobe.

The distribution of chemical signals within aquatic environments is highly patchy and heterogeneous due to dispersion by turbulent eddies. We aimed to quantify the smallest spatial scales associated with chemical patches, and therefore measured the structure of chemical signals under turbulent flow simultaneously at two chemical sensors spaced from 200 to 800 {mu}m apart. Measurements were done under controlled stimulus and flow conditions with a novel semiconductor-based, multisite, microelectrochemical electrode (5-2000 {mu}m2 surface area sensors) and a high-speed computer-based recording system. The chemical signals received at the sensor were intermittent, with wide fluctuations in concentration. Patchiness in signal structure was found at spatial scales as small as 200 {mu}m. Significant differences in signal height were found between recordings made at probes spaced 200, 400, 600, and 800 {mu}m apart. These data demonstrate that sub-millimeter patches occur in aquatic turbulent odor plumes. Such differences in chemical signal structure over small spatial scales might be important for marine animals that employ olfactory orientation. We propose alternative ways by which organisms might deal with these fine scale differences in odor concentration. Animals much larger than microscale patches may have evolved elongated olfactory organs that integrate signals, thereby smoothing variations in sensory input. Animals about the same size as micropatches may be able to capitalize on microscale variation by extracting directional information from turbulent odor plumes.

Ontogeny Versus Phylogeny in Determining Patterns of Chemoreception: Initial Studies with Fiddler Crabs.

Fiddler crab (Uca longisignalis) first stage zoea and adults were assayed for behavioral responses to 16 amino acids and sugars. Larval chemosensitivity was examined using computer-video motion analysis of swimming behavior. Adult sensitivity was assayed by determining the substances that elicit feeding. The pattern of chemoreception expressed by U. longisignalis adults is strongly correlated with that measured previously in adult sand fiddler crabs, Uca pugilator. This concordance among abilities probably reflects shared trophic ecologies of the two species. In contrast, a quantitative analysis shows no significant correlation between the sets of compounds inducing chemoreceptive behavior by larval and adult U. longisignalis. The strongest responses (by both stages) are elicited by substances found in potential prey, and differences in prey types among larvae and adults appear responsible for the lack of correlation. Larvae do, however, respond to substances abundant in prey consumed by adults, even though these substances are absent, or occur at low levels, in larval prey. Adults, on the other hand, appear insensitive to compounds that cue only larval food, but which are maximally stimulatory to larvae. Consequently, our results indicate that the abilities of one life-history stage may be constrained, through development, by the requirements of later stages. The patterns of correlation among adults of different species, and among life-history stages within a species, indicate that both ecological context and developmental factors influence patterns of chemosensitivity.