Common fear molecules induce defensive responses in marine prey across trophic levels.

Predator-prey interactions are a key feature of ecosystems and often chemically mediated, whereby individuals detect molecules in their environment that inform whether they should attack or defend. These molecules are largely unidentified, and their discovery is important for determining their ecological role in complex trophic systems. Homarine and trigonelline are two previously identified blue crab (Callinectes sapidus) urinary metabolites that cause mud crabs (Panopeus herbstii) to seek refuge, but it was unknown whether these molecules influence other species within this oyster reef system. In the current study, homarine, trigonelline, and blue crab urine were tested on juvenile oysters (Crassostrea virginica) to ascertain if the same molecules known to alter mud crab behavior also affect juvenile oyster morphology, thus mediating interactions between a generalist predator, a mesopredator, and a basal prey species. Oyster juveniles strengthened their shells in response to blue crab urine and when exposed to homarine and trigonelline in combination, especially at higher concentrations. This study builds upon previous work to pinpoint specific molecules from a generalist predator's urine that induce defensive responses in two marine prey from different taxa and trophic levels, supporting the hypothesis that common fear molecules exist in ecological systems.

Predator signaling of multiple prey on different trophic levels structures trophic cascades.

The capacity of an apex predator to produce nonconsumptive effects (NCEs) in multiple prey trophic levels can create considerable complexity in nonconsumptive cascading interactions, but these effects are poorly studied. We examined such effects in a model food web where the apex predator (blue crabs) releases chemical cues in urine that affect both the intermediate consumer (mud crabs seek shelter) and the basal prey (oysters are induced to grow stronger shells). Shelter availability and predator presence were manipulated in a laboratory experiment to identify patterns in species interactions. Then, experimentally induced and uninduced oysters were planted across high-quality and low-quality habitats with varying levels of shelter availability and habitat heterogeneity to determine the consistency of these patterns in the field. Oyster shell thickening in response to blue crab chemical cues generally protected oysters from mud crab predation in both the laboratory and in field environments that differed in predation intensity, structural complexity, habitat heterogeneity, and predator composition. However, NCEs on the intermediate predator (greater use of refugia) opposed the NCEs on oyster prey in the interior of oyster reefs while still providing survival advantages to basal prey on reef edges and bare substrates. Thus, the combined effects of changing movement patterns of intermediate predators and morphological defenses of basal prey create complex, but predictable, patterns of NCEs across landscapes and ecotones that vary in structural complexity. Generalist predators that feed on multiple trophic levels are ubiquitous, and their potential effects on NCEs propagating simultaneously to different trophic levels must be quantified to understand the role of NCEs in food webs.

Environmental stress gradients regulate the relative importance of predator density- and trait-mediated indirect effects in oyster reef communities.

Predators affect community structure by influencing prey density and traits, but the importance of these effects often is difficult to predict. We measured the strength of blue crab predator effects on mud crab prey consumption of juvenile oysters across a flow gradient that inflicts both physical and sensory stress to determine how the relative importance of top predator density-mediated indirect effects (DMIEs) and trait-mediated indirect effects (TMIEs) change within systems. Overall, TMIEs dominated in relatively benign flow conditions where blue crab predator cues increased oyster survivorship by reducing mud crab-oyster consumption. Blue crab DMIEs became more important in high sensory stress conditions, which impaired mud crab perception of blue crab chemical cues. At high physical stress, the environment benefitted oyster survival by physically constraining mud crabs. Thus, factors that structure communities may be predicted based on an understanding of how physical and sensory performances change across environmental stress gradients.

Morphology and Surface Properties of Roach Water Transport Arrays.

We report on morphological studies of wharf roaches, Ligia exotica, which can passively absorb and transport water through the microscopic protrusions on their legs. We systematically investigated the geometrical variables of the protrusions on each podite of legs to reveal a particularized structural complexity. For the morphological analysis, each podite was split into nine different zones by grouping the protrusions with similar shapes and organization. The protrusions are shown to possess three different types of shapes located on each specific zone of the podite. In addition, the nanoscale surface morphologies of the protrusions on the wharf roach legs were probed by using atomic force microscopy, and the surface properties of the hairy arrays were determined for identifying the localized hydrophobicity distribution. The protrusion surface possessed a nanoscale periodic patterned texture, and both the valley and ridges of a periodic pattern on the protrusion surface exhibited an identical low surface energy. We suggest that the structural morphologies and distinct hydrophobicity of the protrusions can be critical in determining the directional wettability of an entire leg and important for designing a sturdy water transport and passive water-absorbing system without external energy consumption.

Hydrodynamics affect predator controls through physical and sensory stressors.

Predators influence communities through either consuming prey (consumptive effects, CEs) or altering prey traits (non-consumptive effects, NCEs), which has cascading effects on lower trophic levels. CEs are well known to decrease in physically stressful environments, but NCEs may be reduced at physically benign levels that affect the ability of prey to detect and respond to predators (i.e., sensory stress). We investigated the influence of physical and sensory stressors created by spatial and temporal differences in tidal flow on predator controls in a tritrophic system. We estimated mud crab reactive ranges to blue crab NCEs by evaluating mud crab CEs on juvenile oysters at different distances away from caged blue crabs across flow conditions. Mud crab reactive ranges were large at lower physical and sensory stress levels and blue crabs had a positive cascading effect on oyster survival. Blue crab NCEs were not important at higher flow conditions. Oyster survival was a complicated function of both types of stressors. Physical stress (i.e., current speed) had a positive effect on oyster survival by physically limiting mud crab CEs at high current speeds. Sensory stress (i.e., turbulence) interfered with the propagation of blue crab chemical cues used by mud crabs for predator detection, which removed blue crab NCEs. Mud crab CEs increased as a result and had a negative effect on oyster survival in turbulent conditions. Thus, environmental properties, such as fluid flow, can inflict physical and sensory stressors that have distinct effects on basal prey performance through impacts on different predator effects.

Chemical encoding of risk perception and predator detection among estuarine invertebrates.

An effective strategy for prey to survive in habitats rich in predators is to avoid being noticed. Thus, prey are under selection pressure to recognize predators and adjust their behavior, which can impact numerous community-wide interactions. Many animals in murky and turbulent aquatic environments rely on waterborne chemical cues. Previous research showed that the mud crab, Panopeus herbstii, recognizes the predatory blue crab, Callinectus sapidus, via a cue in blue crab urine. This cue is strongest if blue crabs recently preyed upon mud crabs. Subsequently, mud crabs suppress their foraging activity, reducing predation by blue crabs. Using NMR spectroscopy- and mass spectrometry-based metabolomics, chemical variation in urine from blue crabs fed different diets was related to prey behavior. We identified the urinary metabolites trigonelline and homarine as components of the cue that mud crabs use to detect blue crabs, with concentrations of each metabolite dependent on the blue crab's diet. At concentrations found naturally in blue crab urine, trigonelline and homarine, alone as well as in a mixture, alerted mud crabs to the presence of blue crabs, leading to decreased foraging by mud crabs. Risk perception by waterborne cues has been widely observed by ecologists, but the molecular nature of these cues has not been previously identified. Metabolomics provides an opportunity to study waterborne cues where other approaches have historically failed, advancing our understanding of the chemical nature of a wide range of ecological interactions.

You Are What you Eat: a Metabolomics Approach to Understanding Prey Responses to Diet-Dependent Chemical Cues Released by Predators.

Prey responses to predator cues are graded in intensity in accordance with the degree of threat presented by the predator. In systems in which prey gather information on predators by using chemicals, prey often respond more to the odor of predators that have consumed conspecifics, as opposed to heterospecifics. We investigated the response of a prey species, the mud crab, Panopeus herbstii, to urine of blue crab, Callinectes sapidus, fed mud crabs or oysters. Behavioral analysis was combined with metabolomics to characterize bioactive deterrents in the urine of predators fed different diets. Urine from blue crabs fed oysters or mud crabs depressed mud crab foraging when presented singly, with the urine derived from a mud crab diet being more potent. The magnitude of foraging depression increased with urine concentration. When urine from blue crabs fed oysters or mud crabs was combined, response to the urine mixture was no different from that to urine derived only from a mud crab diet. Metabolomics analysis indicated diet-dependent differences were related to a set of shared spectral features that differed in concentration in the respective urines, likely consisting of aromatic compounds, amino acids, and lipids. Taken together, these results suggest mud crabs distinguish diet of, and therefore the risk imposed by, predators through detection of a suite of compounds that together represent what the predator has recently consumed.

Designing Industrial Networks Using Ecological Food Web Metrics.

Biologically Inspired Design (biomimicry) and Industrial Ecology both look to natural systems to enhance the sustainability and performance of engineered products, systems and industries. Bioinspired design (BID) traditionally has focused on a unit operation and single product level. In contrast, this paper describes how principles of network organization derived from analysis of ecosystem properties can be applied to industrial system networks. Specifically, this paper examines the applicability of particular food web matrix properties as design rules for economically and biologically sustainable industrial networks, using an optimization model developed for a carpet recycling network. Carpet recycling network designs based on traditional cost and emissions based optimization are compared to designs obtained using optimizations based solely on ecological food web metrics. The analysis suggests that networks optimized using food web metrics also were superior from a traditional cost and emissions perspective; correlations between optimization using ecological metrics and traditional optimization ranged generally from 0.70 to 0.96, with flow-based metrics being superior to structural parameters. Four structural food parameters provided correlations nearly the same as that obtained using all structural parameters, but individual structural parameters provided much less satisfactory correlations. The analysis indicates that bioinspired design principles from ecosystems can lead to both environmentally and economically sustainable industrial resource networks, and represent guidelines for designing sustainable industry networks.

The smell of success: the amount of prey consumed by predators determines the strength and range of cascading non-consumptive effects.

We examined whether chemically mediated risk perception by prey and the effects of changes in prey behavior on basal resources vary as a function of the amount of prey biomass consumed by the predator. We studied these issues using a tritrophic system composed of blue crabs, Callinectes sapidus (top predator), mud crabs Panopeus herbstii (intermediate prey), and oysters Crassostrea virginica (basal resource). Working in a well characterized field environment where experiments preserve natural patterns of water flow, we found that biomass consumed by a predator determines the range, intensity and nature of prey aversive responses. Predators that consume large amounts of prey flesh more strongly diminish consumption of basal resources by prey and exert effects over a larger range (in space and time) compared to predators that have eaten less. Less well-fed predators produce weaker effects, with the consequence that behaviorally mediated cascades preferentially occur in refuge habitats. Well-fed predators affected prey behavior and increased basal resources up to distances of 1-1.5 m, whereas predators fed restricted diet evoked changes in prey only when they were extremely close, typically 50 cm or less. Thus, consumptive and non-consumptive effects may be coupled; predators that have a greater degree of predatory success will affect prey traits more strongly and non-consumptive and consumptive effects may fluctuate in tandem, with some lag. Moreover, differences among predators in their degree of prey capture will create spatial and temporal variance in risk cue availability in the absence of underlying environmental effects.

The sensory ecology of nonconsumptive predator effects.

Nonconsumptive effects (NCEs) have been shown to occur in numerous systems and are regarded as important mechanisms by which predation structures natural communities. Sensory ecology-that is, the processes governing the production, propagation, and masking of cues by ambient noise-provides insights into the strength of NCEs as functions of the environment and modes of information transfer. We discuss how properties of predators are used by prey to encode threat, how the environment affects cue propagation, and the role of single sensory processes versus multimodal sensory processes. We discuss why the present body of literature documents the potential for strong NCEs but does not allow us to easily determine how this potential is expressed in nature or what factors or environments produce strong versus weak NCEs. Many of these difficulties stem from a body of literature in which certain sensory environments and modalities may be disproportionately represented and in which experimental methodologies are designed to show the existence of NCEs. We present a general framework for examining NCEs to identify the factors controlling the number of prey that respond to predator cues and discuss how the properties of predators, prey, and the environment may determine prey perceptive range and the duration and frequency of cue production. We suggest how understanding these relationships provides a schema for determining where, when, why, and how NCEs are important in producing direct and cascading effects in natural communities.

Biotic structure indirectly affects associated prey in a predator-specific manner via changes in the sensory environment.

Indirect effects, which can be either positive or negative, may be important in areas containing biotic structure, because such structure can provide refuge and habitat, produce additional sensory cues that may attract predators, and modify the sensory landscape in which predator-prey interactions occur. To determine the indirect effects of biotic structure on prey populations, we assessed predation on patches of hard clams (Mercenaria mercenaria) by large odor-mediated blue crab (Callinectes sapidus) and knobbed whelk (Busycon carica) predators at 0, 5, and 10 m from oyster reefs in intertidal salt marshes. Oyster reefs had an overall indirect negative effect on hard clams, with higher predation rates closer to the reef than farther away. Predator-specific patterns of predation showed that blue crabs consumed more clams very close to the reef, whereas whelks consumed more clams at intermediate distances. Laboratory flume experiments suggest that the oyster reef structure creates turbulence that diminishes predator foraging efficiency, particularly in rapidly mobile predators such as blue crabs, but that oyster reef chemicals ameliorate the negative impact of turbulence on foraging success for both predators. Changes in the sensory landscape, in combination with predator perceptual ability, will determine the positive and/or negative impacts of biotic structure on associated prey. Gaining an understanding of the context specificity of positive and negative sensory effects of biotic structure provides insights that are important for developing a predictive framework to assess the magnitude and distribution of indirect interactions in natural communities.

Predator biomass determines the magnitude of non-consumptive effects (NCEs) in both laboratory and field environments.

Predator body size often indicates predation risk, but its significance in non-consumptive effects (NCEs) and predator risk assessment has been largely understudied. Although studies often recognize that predator body size can cause differing cascading effects, few directly examine prey foraging behavior in response to individual predator sizes or investigate how predator size is discerned. These mechanisms are important since perception of the risk imposed by predators dictates behavioral responses to predators and subsequent NCEs. Here, we evaluate the role of predator body size and biomass on risk assessment and the magnitude of NCEs by investigating mud crab foraging behavior and oyster survival in response to differing biomasses of blue crab predators using both laboratory and field methods. Cues from high predator biomass treatments including large blue crab predators and multiple small blue crab predators decreased mud crab foraging and increased oyster survival, whereas mud crab foraging in response to a single small blue crab did not differ from controls. Mud crabs also increased refuge use in the presence of large and multiple small, but not single small, blue crab predators. Thus, both predator biomass and aggregation patterns may affect the expression of NCEs. Understanding the impact of predator biomass may therefore be necessary to successfully predict the role of NCEs in shaping community dynamics. Further, the results of our laboratory experiments were consistent with observed NCEs in the field, suggesting that data from mesocosm environments can provide insight into field situations where flow and turbulence levels are moderate.

Correlation between thermodynamic efficiency and ecological cyclicity for thermodynamic power cycles.

A sustainable global community requires the successful integration of environment and engineering. In the public and private sectors, designing cyclical ("closed loop") resource networks increasingly appears as a strategy employed to improve resource efficiency and reduce environmental impacts. Patterning industrial networks on ecological ones has been shown to provide significant improvements at multiple levels. Here, we apply the biological metric cyclicity to 28 familiar thermodynamic power cycles of increasing complexity. These cycles, composed of turbines and the like, are scientifically very different from natural ecosystems. Despite this difference, the application results in a positive correlation between the maximum thermal efficiency and the cyclic structure of the cycles. The immediate impact of these findings results in a simple method for comparing cycles to one another, higher cyclicity values pointing to those cycles which have the potential for a higher maximum thermal efficiency. Such a strong correlation has the promise of impacting both natural ecology and engineering thermodynamics and provides a clear motivation to look for more fundamental scientific connections between natural and engineered systems.

Dine or dash? Turbulence inhibits blue crab navigation in attractive-aversive odor plumes by altering signal structure encoded by the olfactory pathway.

Blue crabs can distinguish and navigate to attractive (food) odors even when aversive odors (injured crab metabolites) are released nearby. Blue crabs in these conditions detect the aversive odor and avoid it, but find the attractive source with nearly the same success rate as when the attractive source is presented alone. Spatially and temporally distinct odor filaments appear to signal to foragers that the two odor sources are not co-located, and hence navigating to the attractive odor entails an acceptable risk of predation. However, environmentally produced turbulence suppresses tracking by homogenizing the two odors; blue crabs fail to track to the attractive source when the aversive source is present, even though turbulence does not substantially inhibit tracking to the attractive source alone. Removal of sensory input from aesthetascs on the antennules, but not chemosensors on the legs, rescues navigation to attractive-aversive dual plumes in turbulent conditions. These results suggest that mixing in the natural environment may amplify the effects of predators by suppressing tracking to food odors when aversive cues are present, and that the olfactory pathway mediates the response.

Getting ahead: context-dependent responses to odorant filaments drive along-stream progress during odor tracking in blue crabs.

The chemosensory signal structure governing the upstream progress of blue crabs to an odorant source was examined. We used a three-dimensional laser-induced fluorescence system to collect chemical concentration data simultaneously with behavior observations of actively tracking blue crabs (Callinectes sapidus) in a variety of plume types. This allowed us to directly link chemical signal properties at the antennules and legs to subsequent upstream motion while altering the spatial and temporal intermittency characteristics of the sensory field. Our results suggest that odorant stimuli elicit responses in a binary fashion by causing upstream motion, provided the concentration at the antennules exceeds a specific threshold. In particular, we observed a significant association between crab velocity changes and odorant spike encounters defined using a threshold that is scaled to the mean of the instantaneous maximum concentration. Thresholds were different for each crab, indicating a context-sensitive response to signal dynamics. Our data also indicate that high frequency of odorant spike encounters terminate upstream movement. Further, the data provide evidence that the previous state of the crab and prior stimulus history influence the behavioral response (i.e. the response is context dependent). Two examples are: (1) crabs receiving prior odorant spikes attained elevated velocity more quickly in response to subsequent spikes; and (2) prior acceleration or deceleration of the crab influenced the response time period to a particular odorant spike. Finally, information from both leg and antennule chemosensors interact, suggesting parallel processing of odorant spike properties during navigation.

Staying the course: chemical signal spatial properties and concentration mediate cross-stream motion in turbulent plumes.

This study examined the role of broadly distributed sensor populations in chemosensory searching, especially cross-stream heading adjustment. We used three-dimensional laser-induced fluorescence to collect chemical concentration data simultaneously with behavior observations of actively tracking blue crabs (Callinectes sapidus). Our analysis indicates that the spatial distribution of the odorant concentration field is necessary and sufficient to mediate correct cross-stream motion, although concentration provides information that supplements that obtained from the spatial distribution. Crab movement is continually adjusted to maintain an upstream heading, with corrections toward the source modulated only in the presence of chemical cues. Crabs detect and respond to shifts in the position of the center-of-mass (COM) of the odorant concentration distribution as small as 5% of the leg span, which corresponds to ∼0.8-0.9 cm. The reaction time after a 5% threshold shift in the position of the COM is in the range of 2-4 s. Data also indicate that these steering responses are dependent on stimulus history or other characteristics of the plume, with crabs taking longer to respond in conditions with large-scale spatial meanders. Although cross-stream motion is determined by chemical signal inputs to receptors on the walking legs, crabs do make rotational movements in response to chemical signals impinging on the antennules. These rotational movements do not affect the direction of travel, but rather, determine the crab's body angle with respect to the flow. Interestingly, these body angles seem to represent a compromise between reducing drag and obtaining better chemical signal information, and this trade-off is resolved differently under different plume conditions.

Hydrodynamic sensory stressors produce nonlinear predation patterns.

Predators often have large effects on community structure, but these effects can be minimized in habitats subjected to intense physical stress. For example, predators exert large effects on rocky intertidal communities on wave-protected shores but are usually absent from wave-swept shores where hydrodynamic forces prevent them from foraging effectively. The physical environment also can affect predation levels when stressors are not severe enough to be physically risky. In these situations, environmental conditions may constrain a predator's ability to locate prey and alleviate predation pressure. Yet, stress models of community structure have rarely considered the implications of such sensory or behavioral stressors, particularly when the sensory abilities of both predators and prey are affected by the same types of environmental conditions. Ecologists may classify certain environmental conditions as refuges if they impede predator foraging, but these conditions may not actually decrease predation levels if they simultaneously increase prey vulnerability to consumers. Using blue crabs (Callinectes sapidus) and hard clams (Mercenaria mercenaria) as a model system, we investigated the relationship between predation intensity and environmental stress in the form of hydrodynamics (i.e., flow velocity and turbulence). Blue crabs and hard clams are less responsive to each other in faster, more turbulent flows, but studies exploring how flow modulates the outcomes of crab-clam interactions in the field are lacking. We manipulated turbulence within field sites and compared predation levels within and between sites that differed in flow velocity and turbulence. Our results suggest that blue crabs are most effective foragers in flows with intermediate velocities and turbulence levels. Although these conditions are not ideal for blue crabs, lab studies indicate that they also compromise the ability of clams to detect and react to approaching crabs and, thereby, increase clam vulnerability to predators. Our results suggest that environmental stresses on perception (sensory stressors) may not cause a steady decay in predation rates when they simultaneously affect the behaviors of both predators and prey. Moreover, the relative contribution of lethal vs. nonlethal predator effects in communities also may be influenced by environmental forces that enhance the predator-avoidance abilities of prey or the foraging efficiency of predators.

Alteration of sensory abilities regulates the spatial scale of nonlethal predator effects.

Many studies have shown that nonlethal predator effects such as trait-mediated interactions (TMIs) can have significant impacts on the structure and function of communities, but the role that environmental conditions play in modulating the scale and magnitude of these effects has not been carefully investigated. TMIs occur when prey exhibit behavioral or physiological responses to predators and may be more prevalent when abiotic conditions increase prey reactions to consumers. The purpose of this study was to determine if turbulence would alter the distance over which prey in aquatic systems respond to chemical cues emitted by predators in nature, thus changing the scales over which nonlethal predator effects occur. Using hard clams and blue crabs as a model predator-prey system, we investigated the effects of turbulence on clam reactive distance to predatory blue crabs in the field. Results suggest that turbulence diminishes clam reactions to predators and that the environmental context must be considered when predicting the extent of indirect predator effects in natural systems.

The olfactory pathway mediates sheltering behavior of Caribbean spiny lobsters, Panulirus argus, to conspecific urine signals.

The "noses" of diverse taxa are organized into different subsystems whose functions are often not well understood. The "nose" of decapod crustaceans is organized into two parallel pathways that originate in different populations of antennular sensilla and project to specific neuropils in the brain-the aesthetasc/olfactory lobe pathway and the non-aesthetasc/lateral antennular neuropil pathway. In this study, we investigated the role of these pathways in mediating shelter selection of Caribbean spiny lobsters, Panulirus argus, in response to conspecific urine signals. We compared the behavior of ablated animals and intact controls. Our results show that control and non-aesthetasc ablated lobsters have a significant overall preference for shelters emanating urine over control shelters. Thus the non-aesthetasc pathway does not play a critical role in shelter selection. In contrast, spiny lobsters with aesthetascs ablated did not show a preference for either shelter, suggesting that the aesthetasc/olfactory pathway is important for processing social odors. Our results show a difference in the function of these dual chemosensory pathways in responding to social cues, with the aesthetasc/olfactory lobe pathway playing a major role. We discuss our results in the context of why the noses of many animals contain multiple parallel chemosensory systems.