Automated escape system: identifying prey's kinematic and behavioral features critical for predator evasion.

Identifying the kinematic and behavioral variables of prey that influence evasion from predator attacks remains challenging. To address this challenge, we have developed an automated escape system that responds quickly to an approaching predator and pulls the prey away from the predator rapidly, similar to real prey. Reaction distance, response latency, escape speed and other variables can be adjusted in the system. By repeatedly measuring the response latency and escape speed of the system, we demonstrated the system's ability to exhibit fast and rapid responses while maintaining consistency across successive trials. Using the live predatory fish species Coreoperca kawamebari, we show that escape speed and reaction distance significantly affect the outcome of predator-prey interactions. These findings indicate that the developed escape system is useful for identifying kinematic and behavioral features of prey that are critical for predator evasion, as well as for measuring the performance of predators.

Crop Diversity in Agroecosystems for Pest Management and Food Production.

During the past 30 years, there has been a growing belief in and promotion of agroecosystem diversity for pest management and future food production as an agroecological or nature-based approach. Monoculture agriculture, which produces most of our food, is considered to be highly vulnerable to pests in contrast to plant species-diverse agroecosystems which may possess a greater abundance of natural enemies, keeping pest populations under control. In this paper, we question the role of crop diversity for pest management and explore the relationship between crop and associated diversity and pests through the following processes: environmental stresses that favor monodominance; evolutionary adaptations that resist insect herbivores (genetic resistance response); mechanisms of spatial escape from insect herbivores (escape response); and the role of crop-associated biodiversity. We present strong evidence that not only questions the high vulnerability of monocultures to pest damage but also supports why monocultures continue to produce most of the world's food. Reference is made to the importance of targeted plant breeding and the role of trans-continental crop introduction supported by efficient quarantine for pest management. We conclude that-with the exception of irrigated rice-much more research is needed to better understand the role of crop diversity in agroecosystems for pest management and food production.

Use of acoustic stimulus to determine behavioral changes in zebrafish after Cd exposure in a water quality warning system.

Behavioral changes in zebrafish are an effective early warning system to determine water quality. However, only a few studies have examined the response of zebrafish to non-chemical stimulus after exposure to a contaminant. Therefore, this study investigated the differences in the behavioral responses of zebrafish to acoustic stimuli before and after exposure to cadmium (Cd). Acoustic escape response sensitivity curves were obtained and analyzed, followed by the determination of sensitive stimulus conditions at 100 Hz and 97 dB with a duration of 30 s and an interval of 30 min. Zebrafish exhibit a significant acoustic escape response, which is significantly reduced after exposure to Cd. The results showed that zebrafish stop demonstrating acoustic escape responses when exposed to higher Cd concentrations or longer acoustic exposures. Based on these results, a novel method for detecting abnormal behavior in zebrafish by acoustic stimulation has been proposed, which is expected to reduce the false alarm rate of this type of water quality technology.

Evidence for Prepulse Inhibition of Visually Evoked Motor Response in Drosophila melanogaster.

Prepulse inhibition (PPI) is a widely investigated behavior to study the mechanisms of disorders such as anxiety, schizophrenia, and bipolar mania. PPI has been observed across various vertebrate and invertebrate species; however, it has not yet been reported in adult Drosophila melanogaster. In this study, we describe the first detection of PPI of visually evoked locomotor arousal in flies. To validate our findings, we demonstrate that PPI in Drosophila can be partially reverted by the N-methyl D-aspartate (NMDA) receptor antagonist MK-801, known for inducing sensorimotor gating deficits in rodent models. Additionally, we show that the visually evoked response can be inhibited by multiple stimuli presentation, which can also be affected by MK-801. Given the versatility of Drosophila as a model organism for genetic screening and analysis, our results suggest that high-throughput behavioral screenings of adult flies can become a valuable tool for investigating the mechanisms behind PPI.

Multiple preferred escape trajectories are explained by a geometric model incorporating prey's turn and predator attack endpoint.

The escape trajectory (ET) of prey - measured as the angle relative to the predator's approach path - plays a major role in avoiding predation. Previous geometric models predict a single ET; however, many species show highly variable ETs with multiple preferred directions. Although such a high ET variability may confer unpredictability to avoid predation, the reasons why animals prefer specific multiple ETs remain unclear. Here, we constructed a novel geometric model that incorporates the time required for prey to turn and the predator's position at the end of its attack. The optimal ET was determined by maximizing the time difference of arrival at the edge of the safety zone between the prey and predator. By fitting the model to the experimental data of fish Pagrus major, we show that the model can clearly explain the observed multiple preferred ETs. By changing the parameters of the same model within a realistic range, we were able to produce various patterns of ETs empirically observed in other species (e.g., insects and frogs): a single preferred ET and multiple preferred ETs at small (20-50°) and large (150-180°) angles from the predator. Our results open new avenues of investigation for understanding how animals choose their ETs from behavioral and neurosensory perspectives.

When a prey spots a predator about to pounce, it turns swiftly and accelerates away to avoid being captured. The initial direction the prey chooses to take ­ known as its escape trajectory ­ can greatly impact their chance of survival. Previous models were able to predict the optimal direction an animal should take to maximize its chances of evading the predator. However, experimental data suggest that prey actually tend to escape via multiple specific directions, although why animals use this approach has not been clarified. To investigate this puzzle, Kawabata et al. built a new mathematical model that better represents how prey and predators interact with one another in the real world. Unlike past models, Kawabata et al. incorporated the time required for prey to change direction and only allowed the predators to move toward the prey for a limited distance. By including these two factors, they were able to reproduce the escape trajectories of real animals, including a species of fish, as well as species from other taxa such as frogs and insects. The new model suggests that prey escape along one of two directions: either by moving directly away from the predator in order to outrun its attack, or by dodging sideways to avoid being captured. Which strategy the prey chooses has some elements of unpredictability, which makes it more difficult for predators to adjust their capturing method. These findings shed light on why escaping in multiple specific directions makes prey harder to catch. The model could also be extended to test the escape trajectories of a wider variety of predator and prey species, which may avoid capture via different routes. This could help researchers better understand how predators and prey interact with one another. The findings could also reveal how sensory information (such as sound and sight) associated with the threat of an approaching predator is processed and stimulates the muscle activity required to escape in multiple different directions.

Isopod parasite influences prawn responsiveness and activity.

Most bopyrid isopod parasites, which are crustaceans themselves, settle in the branchial chamber of decapod crustaceans and feed on host haemolymph. Here we report the results of an experiment on the common prawn Palaemon serratus and the parasite Bopyrus squillarum. Infected and uninfected prawns were stimulated with pokes of a plastic rod until an escape response was triggered; the number of pokes was recorded as an indicator of prawn responsiveness, whereas the time spent moving following stimulation was used as an indicator of prawn activity. Our results show that bopyrid infection affects both prawn responsiveness and activity, with infected prawns requiring more pokes to move, and moving for less time compared to uninfected prawns. In nature, such behavioural changes may impact defence mechanisms and survival of infected prawns. This could contribute to decreases in P. serratus abundance, thereby affecting the coastal ecosystems home to this species and the fisheries reliant on it, such as the Irish shrimp fishery.

Increased parasite load is associated with reduced metabolic rates and escape responsiveness in pumpkinseed sunfish.

Wild animals have parasites that can compromise their physiological and/or behavioural performance. Yet, the extent to which parasite load is related to intraspecific variation in performance traits within wild populations remains relatively unexplored. We used pumpkinseed sunfish (Lepomis gibbosus) and their endoparasites as a model system to explore the effects of infection load on host aerobic metabolism and escape performance. Metabolic traits (standard and maximum metabolic rates, aerobic scope) and fast-start escape responses following a simulated aerial attack by a predator (responsiveness, response latency and escape distance) were measured in fish from across a gradient of visible (i.e. trematodes causing black spot disease counted on fish surfaces) and non-visible (i.e. cestodes in fish abdominal cavity counted post-mortem) endoparasite infection. We found that a higher infection load of non-visible endoparasites was related to lower standard and maximum metabolic rates, but not aerobic scope in fish. Non-visible endoparasite infection load was also related to decreased responsiveness of the host to a simulated aerial attack. Visible endoparasites were not related to changes in metabolic traits or fast-start escape responses. Our results suggest that infection with parasites that are inconspicuous to researchers can result in intraspecific variation in physiological and behavioural performance in wild populations, highlighting the need to more explicitly acknowledge and account for the role played by natural infections in studies of wild animal performance.

Escaping from multiple visual threats: modulation of escape responses in Pacific staghorn sculpin (Leptocottus armatus).

Fish perform rapid escape responses to avoid sudden predatory attacks. During escape responses, fish bend their bodies into a C-shape and quickly turn away from the predator and accelerate. The escape trajectory is determined by the initial turn (stage 1) and a contralateral bend (stage 2). Previous studies have used a single threat or model predator as a stimulus. In nature, however, multiple predators may attack from different directions simultaneously or in close succession. It is unknown whether fish are able to change the course of their escape response when startled by multiple stimuli at various time intervals. Pacific staghorn sculpin (Leptocottus armatus) were startled with a left and right visual stimulus in close succession. By varying the timing of the second stimulus, we were able to determine when and how a second stimulus could affect the escape response direction. Four treatments were used: a single visual stimulus (control); or two stimuli coming from opposite sides separated by a 0 ms (simultaneous treatment), 33 ms or 83 ms time interval. The 33 ms and 83 ms time intervals were chosen to occur either side of a predicted 60 ms visual escape latency (i.e. during stage 1). The 0 ms and 33 ms treatments influenced both the escape trajectory and the stage 1 turning angle, compared with a single stimulation, whereas the 83 ms treatment had no effect on the escape trajectory. We conclude that Pacific staghorn sculpin can modulate their escape trajectory only between stimulation and the onset of the response, but the escape trajectory cannot be modulated after the body motion has started.

The scent of fear makes sea urchins go ballistic.

BACKGROUND: Classic ecological formulations of predator-prey interactions often assume that predators and prey interact randomly in an information-limited environment. In the field, however, most prey can accurately assess predation risk by sensing predator chemical cues, which typically trigger some form of escape response to reduce the probability of capture. Here, we explore under laboratory-controlled conditions the long-term (minutes to hours) escaping response of the sea urchin Paracentrotus lividus, a key species in Mediterranean subtidal macrophyte communities. METHODS: Behavioural experiments involved exposing a random sample of P. lividus to either one of two treatments: (i) control water (filtered seawater) or (ii) predator-conditioned water (with cues from the main P. lividus benthic predator-the gastropod Hexaplex trunculus). We analysed individual sea urchin trajectories, computed their heading angles, speed, path straightness, diffusive properties, and directional entropy (as a measure of path unpredictability). To account for the full picture of escaping strategies, we followed not only the first instants post-predator exposure, but also the entire escape trajectory. We then used linear models to compare the observed results from control and predators treatments. RESULTS: The trajectories from sea urchins subjected to predator cues were, on average, straighter and faster than those coming from controls, which translated into differences in the diffusive properties and unpredictability of their movement patterns. Sea urchins in control trials showed complex diffusive properties in an information-limited environment, with highly variable trajectories, ranging from Brownian motion to superdiffusion, and even marginal ballistic motion. In predator cue treatments, variability reduced, and trajectories became more homogeneous and predictable at the edge of ballistic motion. CONCLUSIONS: Despite their old evolutionary origin, lack of cephalization, and homogenous external appearance, the trajectories that sea urchins displayed in information-limited environments were complex and ranged widely between individuals. Such variable behavioural repertoire appeared to be intrinsic to the species and emerged when the animals were left unconstrained. Our results highlight that fear from predators can be an important driver of sea urchin movement patterns. All in all, the observation of anomalous diffusion, highly variable trajectories and the behavioural shift induced by predator cues, further highlight that the functional forms currently used in classical predator-prey models are far from realistic.

Habituation in Aedes aegypti mosquito larvae is context specific.

Mosquito larvae live in water and perform a stereotyped escape response when a moving object projects its shadow on the water surface, indicating potential risk of predation. Repeated presentations of the shadow induce a decrease in the response as a result of habituation, a form of non-associative learning defined as the progressive and reversible decrease in response to a specific reiterative innocuous stimulus. Nevertheless, habituation can be context specific, which indicates an association between the context and the stimulus. The aim of this work was to study context specificity in habituation in mosquito larvae Aedes aegypti. Larvae were individually placed in Petri dishes positioned over black, white or black-white striped cardboard as background (visual context). Larvae were presented with a shadow produced by a cardboard square (training) over the course of 15 trials. After the 15th trial, the background was changed and the stimulus was presented once again (test). To analyse habituation in different contexts, we developed a series of learning curve models. We performed a Bayesian model selection procedure using those models and the data from the experiments to find which model best described the results. The selected model was a power law learning curve with six parameters (habituation rate; context-specific asymptotic habituation response, with one parameter per context, i.e. 3 parameters in total; response increase; and autocorrelation) describing the whole experimental setup with a generalised r2 of 0.96. According to the model, a single habituation rate would indicate that habituation was independent of the context, whilst asymptotic habituation would be context specific. If the background was changed after training, there was an increase in response in the test, evincing context specificity in habituation.

Developmental Exposure to Domoic Acid Disrupts Startle Response Behavior and Circuitry in Zebrafish.

Harmful algal blooms produce potent neurotoxins that accumulate in seafood and are hazardous to human health. Developmental exposure to the harmful algal bloom toxin, domoic acid (DomA), has behavioral consequences well into adulthood, but the cellular and molecular mechanisms of DomA developmental neurotoxicity are largely unknown. To assess these, we exposed zebrafish embryos to DomA during the previously identified window of susceptibility and used the well-known startle response circuit as a tool to identify specific neuronal components that are targeted by exposure to DomA. Exposure to DomA reduced startle responsiveness to both auditory/vibrational and electrical stimuli, and even at the highest stimulus intensities tested, led to a dramatic reduction of one type of startle (short-latency c-starts). Furthermore, DomA-exposed larvae had altered kinematics for both types of startle responses tested, exhibiting shallower bend angles and slower maximal angular velocities. Using vital dye staining, immunolabeling, and live imaging of transgenic lines, we determined that although the sensory inputs were intact, the reticulospinal neurons required for short-latency c-starts were absent in most DomA-exposed larvae. Furthermore, axon tracing revealed that DomA-treated larvae also showed significantly reduced primary motor neuron axon collaterals. Overall, these results show that developmental exposure to DomA targets large reticulospinal neurons and motor neuron axon collaterals, resulting in measurable deficits in startle behavior. They further provide a framework for using the startle response circuit to identify specific neural populations disrupted by toxins or toxicants and to link these disruptions to functional consequences for neural circuit function and behavior.

Evolvability under climate change: Bone development and shape plasticity are heritable and correspond with performance in Arctic charr (Salvelinus alpinus).

Environmental conditions can impact the development of phenotypes and in turn the performance of individuals. Climate change, therefore, provides a pressing need to extend our understanding of how temperature will influence phenotypic variation. To address this, we assessed the impact of increased temperatures on ecologically significant phenotypic traits in Arctic charr (Salvelinus alpinus). We raised Arctic charr at 5°C and 9°C to simulate a predicted climate change scenario and examined temperature-induced variation in ossification, bone metabolism, skeletal morphology, and escape response. Fish reared at 9°C exhibited less cartilage and bone development at the same developmental stage, but also higher bone metabolism in localized regions. The higher temperature treatment also resulted in significant differences in craniofacial morphology, changes in the degree of variation, and fewer vertebrae. Both temperature regime and vertebral number affected escape response performance, with higher temperature leading to decreased latency. These findings demonstrate that climate change has the potential to impact development through multiple routes with the potential for plasticity and the release of cryptic genetic variation to have strong impacts on function through ecological performance and survival.

Factors modulating the behavioral and physiological stress responses: Do they modify the relationship between flight initiation distance and corticosterone reactivity?

Understanding how vulnerable species are to new stressors, such as anthropogenic changes, is crucial for mitigating their potential negative consequences. Many studies have investigated species sensitivity to human disturbance by focusing on single behavioral or physiological parameters, such as flight initiation distance and glucocorticoid levels. However, little is known about the differential effect that modulating factors might have on behavioral versus physiological stress responses across species. This lack of knowledge make difficult to understand the relationship between both types of reactions, and thus to assess to what extent a behavioral reaction is representative of an internal physiological stress response or vice versa. We collected published data on bird flight initiation distances (FID) and corticosterone (CORT) responses, the two most frequently used indicators of stress reaction. We then investigated how spatio-temporal factors or species-specific characteristics relate to these behavioral and physiological stress responses, and potentially modify the relationship between them. Additionally, we evaluated the strength of the correlation between the two stress responses (behavioral and physiological). Our findings showed that FID and CORT responses were poorly correlated across species, and the lack of correlation was attributable to modulating factors (e.g. latitude and body mass) which influence behavior and physiology differently. These modulating factors, therefore, should be taken into consideration to better interpret FID and CORT responses in the context of species vulnerability to stress.

Bio-Inspired Architectures Substantially Reduce the Memory Requirements of Neural Network Models.

We propose a neural network model for the jumping escape response behavior observed in the cricket cercal sensory system. This sensory system processes low-intensity air currents in the animal's immediate environment generated by predators, competitors, and mates. Our model is inspired by decades of physiological and anatomical studies. We compare the performance of our model with a model derived through a universal approximation, or a generic deep learning, approach, and demonstrate that, to achieve the same performance, these models required between one and two orders of magnitude more parameters. Furthermore, since the architecture of the bio-inspired model is defined by a set of logical relations between neurons, we find that the model is open to interpretation and can be understood. This work demonstrates the potential of incorporating bio-inspired architectural motifs, which have evolved in animal nervous systems, into memory efficient neural network models.

Turning away from danger.

The flexible escape behavior exhibited by C. elegans in response to threats relies on a combination of feedback and feedforward circuits.

A high-throughput assay for screening environmental pollutants and drugs impairing predator avoidance in Daphnia magna.

This study addresses short-term habituation of the escape response in the aquatic crustacean Daphnia magna evoked by sudden changes in light intensity, using a high-throughput system. Daphnia magna exhibits a marked phototactic behaviour and swim away from light to avoid predation by fish. Currently, there is no information available on the habituation of this phototactic response. The Daphnia photomotor response assay (DPRA) measures the distance moved after a sudden increase in light intensity. Using DPRA, it is possible to determine not only the magnitude of the phototactic response, but also its habituation after repetitive cycles of light and darkness. The progressive reduction observed in response to a series of light stimuli in the proposed assay meet the criteria for habituation. Most cholinergic and serotonergic modulators enhanced photomotor responses and reduced habituation. Dopaminergic and histaminergic modulators also reduced habituation, whereas diazepam was the only compound that increased habituation. Imidacloprid, apomorphine, diphenhydramine, diazepam, and memantine decreased photomotor responses. Thus, the DPRA was also predictive in assessing the effects of neuroactive and neurotoxic environmental contaminants such as selective serotonin reuptake inhibitors, diazepam, organophosphorous, and neonicotinoid pesticides. We conclude that the proposed DPRA may be an effective screening tool for compounds that can impair predation avoidance behaviour in aquatic organisms.

Flexible motor sequence generation during stereotyped escape responses.

Complex animal behaviors arise from a flexible combination of stereotyped motor primitives. Here we use the escape responses of the nematode Caenorhabditis elegans to study how a nervous system dynamically explores the action space. The initiation of the escape responses is predictable: the animal moves away from a potential threat, a mechanical or thermal stimulus. But the motor sequence and the timing that follow are variable. We report that a feedforward excitation between neurons encoding distinct motor states underlies robust motor sequence generation, while mutual inhibition between these neurons controls the flexibility of timing in a motor sequence. Electrical synapses contribute to feedforward coupling whereas glutamatergic synapses contribute to inhibition. We conclude that C. elegans generates robust and flexible motor sequences by combining an excitatory coupling and a winner-take-all operation via mutual inhibition between motor modules.

Roles of Adenylate Cyclases in Ciliary Responses of Paramecium to Mechanical Stimulation.

Paramecium shows rapid forward swimming due to increased beat frequency of cilia in normal (forward swimming) direction in response to various kinds of stimuli applied to the cell surface that cause K+ -outflow accompanied by a membrane hyperpolarization. Some adenylate cyclases are known to be functional K+ channels in the membrane. Using gene-specific knockdown methods, we examined nine paralogues of adenylate cyclases in P. tetraurelia to ascertain whether and how they are involved in the mechanical stimulus-induced hyperpolarization-coupled acceleration of forward swimming. Results demonstrated that knockdown of the adenylate cyclase 1 (ac1)-gene and 2 (ac2)-gene inhibited the acceleration of forward swimming in response to mechanical stimulation of the cell, whereas that spared the acceleration response to external application of 8-Br-cAMP and dilution of extracellular [K+ ] induced hyperpolarization. Electrophysiological examination of the knockdown cells revealed that the hyperpolarization-activated inward K+ current is smaller than that of a normal cell. Our results suggest that AC1 and AC2 are involved in the mechanical stimulus-induced acceleration of ciliary beat in Paramecium.

Size-dependent locomotory performance creates a behaviorally mediated prey size refuge in the marine snail Olivella semistriata: a study in the natural habitat.

The effects of the variability of individual prey locomotory performance on the vulnerability to predation are poorly understood, partly because individual performance is difficult to determine in natural habitats. To gain insights into the role(s) of individual variation in predatory relationships, we study a convenient model system, the neotropical sandy beach gastropod Olivella semistriata and its main predator, the carnivorous snail Agaronia propatula. The largest size class of O. semistriata is known to be missing from A. propatula's spectrum of subdued prey, although the predator regularly captures much larger individuals of other taxa. To resolve this conundrum, we analyzed predation attempts in the wild. While A. propatula attacked O. semistriata of all sizes, large prey specimens usually escaped by 'sculling', an accelerated, stepping mode of locomotion. Olivella semistriata performed sculling locomotion regardless of size, but sculling velocities determined in the natural environment increased strongly with size. Thus, growth in size as such does not establish a prey size refuge in which O. semistriata is safe from predation. Rather, a behaviorally mediated size refuge is created through the size-dependence of sculling performance. Taken together, this work presents a rare quantitative characterization in the natural habitat of the causal sequence from the size-dependence of individual performance, to the prey size-dependent outcome of predation attempts, to the size bias in the predator's prey spectrum.

Sleep deprivation and adrenalectomy lead to enhanced innate escape response to visual looming stimuli.

Optimal selections of innate behaviors that enable animals to adapt to particular conditions, whether environmental or internal, remain poorly understood. We report that mice under acute (8 h) sleep deprivation had an enhanced innate escape response and upregulation of c-fos expression in multiple brain areas that regulate wakefulness. By comparison, adrenalectomized mice under the same sleep deprivation condition displayed an even more exaggerated escape response and these wake-regulating brain areas were even more active. This suggests that acute sleep deprivation enhances innate escape response, possibly by altering wake state without causing significant anxiety. We also report that the hypothalamic-pituitary-adrenal axis feedback under sleep deprivation prevents an exaggerated escape response by modulating wake-regulating brain areas. Taken together, our findings suggest that animals prioritize escape response over sleep, as the need of both behaviors simultaneously increase. We also provide an insight into the neural mechanisms underlying the interaction between sleep and innate escape response.