Predatory Strikes Research Articles

Cold kiss still hot: limited temperature effects on envenomation performance in predatory strikes of a Japanese pit viper (Gloydius blomhoffii).

Understanding how environmental factors affect the performance of predators can provide profound insights into predator-prey interactions from evolutionary and ecological perspectives and the global distributional patterns of each taxon. Almost all venomous predators are ectotherms, with muscle contraction properties depending on temperature. For predators having venom transportation systems driven by muscle contraction, temperature may have quite large effects on envenomation performance for prey subjugation. Here, we used videography and enzyme-linked immunosorbent assay to examine thermal effects on envenomation kinematics and venom expenditure in predatory strikes of a venomous snake, the Mamushi Gloydius blomhoffii, to its main rodent prey at various body temperatures under both field and laboratory experimental conditions. Unexpectedly, we found that the thermal effects on envenomation performance are limited over nearly the entire ecologically relevant range of temperature (from 13.2°C to 26.2°C). Although temperature statistically significantly affected the mass of venom injected under field conditions, temperature explained only a minor proportion of the variation in venom expenditure. These findings suggest that the Mamushi is able to maintain prey subjugation performance across a wide range of temperatures, which is highly advantageous for ectothermic predators. Further studies should examine the underlying mechanisms of the limited thermal effects and their ubiquity across venomous predators.

The matador bug’s elaborate flags deter avian predators

Abstract Large, conspicuous traits frequently evolve despite increased predator attention, but in some cases, specifically to attract attention. Sexually selected traits provide some of the clearest examples of elaboration, yet natural selection can also be a powerful driver. The matador bug, Anisoscelis alipes (Hemiptera: Coreidae), has large, colorful flags on its hindlegs that, unlike many other coreid species, are not used in reproductive competition. We hypothesized that these flags either 1) warn predators of chemical defense or 2) deflect predatory attack to the removable hindlegs. We pitted matador bugs with or without flags and crickets (Acheta domesticus) with or without bug flags experimentally attached to their legs, against live motmot bird predators (Momotus subrufescens and Electron platyrhynchum). Contrary to the deflection hypothesis, almost none of the predatory strikes were directed at hindleg flags. Instead, we found support for the aposematism hypothesis: matador bug flags reduced attacks on palatable crickets but were unnecessary to prevent predator attacks against matador bugs. Palatability studies with naïve chicks (Gallus gallus) further supported a chemical defense hypothesis. Thus, these elaborate hindleg flags serve an aposematic anti-predator function, but in their absence, birds use alternative cues. These findings add to our understanding of the role of predation in driving the evolution of elaborate morphological structures.

A switchable joint in the head of dragonfly larvae (Insecta: Odonata) as key to the multifunctionality of the prehensile labial mask.

Dragonfly and damselfly larvae (Insecta: Odonata) capture prey by rapid protraction of a raptorial mouthpart, based on a modified labium. Yet, in insects with biting-chewing mouthparts, the labium has an essential role in food handling. These two distinct functions -prey capturing and handling-lead to a mechanical problem in Odonata larvae: while the labium is always protracted in a straight line during prey capture, food handling requires more dexterity. In this study, we investigate the role of the labium in the feeding process and analyse the mechanics of the labial joints in the dragonfly larva Anax imperator. Our results show that the labium features a multiaxial joint connecting the basal segment (postmentum) and the head. During feeding, a combination of rotations around different axes is used to handle and orient prey, which is unique among biting-chewing mouthparts. Furthermore, we identified structures at the joint which likely restrict lateral motion during the predatory strike. Our results provide a further understanding of the unique prey-capturing apparatus of odonate larvae capable of controlling a 'switchable' multiaxial to a restricted monoaxial joint. This concept highlights the evolution of a highly modified raptorial mouthpart appendage where the degrees of freedom can be actively restricted to allow for the respectively needed functionality.

Extrinsic and intrinsic musculature of the raptorial forelegs in Mantodea (Insecta) in the light of functionality and sexual dimorphism.

Prehensile raptorial forelegs are prey capturing and grasping devices, best known for praying mantises (Mantodea) within insects. They show strong morphological and behavioral adaptations towarda lifestyle as generalist arthropod predators. In the past, few species of Mantodea were investigated, concerning morphological variability of the raptorial forelegs. Especially the knowledge of foreleg anatomy in the light of functional and comparative morphology is scarce. Our comparative approach is based on the, for arthropods very common, "female-biased sexual size dimorphism"(SSD) that occurs in almost every Mantodea species. Within Mantodea, this SSD is likely leading to a shift of the exploited ecological niche between male and female individuals due to changes in, for example, the possible prey size; which might be reflected in the chosen ecomorphs. In this context, we analyzed the musculature of the raptorial forelegs of female and male specimens in five different species with varying SSD, using high-resolution microcomputed tomography and dissection. We were able to confirm the presence of 15 extrinsic and 15 intrinsic muscles-including one previously undescribed muscle present in all species. Thus, presenting a detailed description and illustrative three-dimensional anatomical visualization of the musculature in Mantodea. Interestingly, almost no observable differences were found, neither between species, nor between the sexes. Furthermore, we homologized all described muscles, due to their attachment points, to the comprehensive nomenclature established by Friedrich and Beutel (2008), discussed potential functionality of the muscles and possible homologies to the neuropteran Mantispa styriaca (Büsse et al., 2021) and the newly introduced leg nomenclature by Aibekova et al. (2022). By elucidating the anatomy, particularly in the context of functionality and SSD, our results complement previous knowledge of the raptorial forelegs, and facilitate a better understanding of the underlying biomechanical system of the predatory strike, and ultimately, a future comparison to other insect taxa.

Roles of muscle activities in foreleg movements during predatory strike of the mantis

Foreleg trajectory in the mantis strike varies depending on prey distance. To examine how muscle activities affect foreleg trajectory, we recorded strike behaviours of the Chinese mantis with a high-speed camera and electromyograms of the foreleg trochanteral extensor and flexor. At the approach phase of the mantis strike, the prothorax–coxa (P–C) joint elevated and the femur–tibia (F–T) joint extended. At the sweep phase, the coxa–trochanter (C–T) joint rapidly extended, then, the F–T joint rapidly flexed to capture the prey. At capture initiation, the C–T joint extended more with greater prey distance. After cutting the tendon of the trochanteral flexor, the C–T joint extended similarly to that of the intact foreleg but did not flex after it reached its peak angle. After cutting the tendon of the trochanteral extensor, the C–T joint did not extend as much as that of the intact foreleg. During rapid extension of the C–T joint, a burst of spikes from the coxal trochanteral extensor was observed in electromyograms. Among several parameters, burst duration was the best predictor of C–T joint angular change during strike. Unexpectedly, trochanteral flexor activity was also observed during rapid extension of the C–T joint. These results indicated that the coxal trochanteral extensor mainly contributed to the rapid C–T extension during strike, but other muscles also contributed at the beginning of extension. The trochanteral flexor appeared to contribute to C–T flexion by countering the rapid extension.

Ecological analysis of Pavlovian fear conditioning in rats

Pavlovian fear conditioning, which offers the advantage of simplicity in both the control of conditional and unconditional stimuli (CS, US) presentation and the analysis of specific conditional and unconditional responses (CR, UR) in a controlled laboratory setting, has been the standard model in basic and translational fear research. Despite 100 years of experiments, the utility of fear conditioning has not been trans-situationally validated in real-life contexts. We thus investigated whether fear conditioning readily occurs and guides the animal’s future behavior in an ecologically-relevant environment. To do so, Long-Evans rats foraging for food in an open arena were presented with a tone CS paired with electric shock US to their dorsal neck/body that instinctively elicited escape UR to the safe nest. On subsequent test days, the tone-shock paired animals failed to exhibit fear CR to the CS. In contrast, animals that encountered a realistic agent of danger (a looming artificial owl) paired with a shock, simulating a plausible predatory strike, instantly fled to the nest when presented with a tone for the first time. These results highlight the possibility of a nonassociative, rather than standard associative, fear process providing survival function in life-threatening situations that animals are likely to encounter in nature.

A computational model of stereoscopic prey capture in praying mantises.

We present a simple model which can account for the stereoscopic sensitivity of praying mantis predatory strikes. The model consists of a single “disparity sensor”: a binocular neuron sensitive to stereoscopic disparity and thus to distance from the animal. The model is based closely on the known behavioural and neurophysiological properties of mantis stereopsis. The monocular inputs to the neuron reflect temporal change and are insensitive to contrast sign, making the sensor insensitive to interocular correlation. The monocular receptive fields have a excitatory centre and inhibitory surround, making them tuned to size. The disparity sensor combines inputs from the two eyes linearly, applies a threshold and then an exponent output nonlinearity. The activity of the sensor represents the model mantis’s instantaneous probability of striking. We integrate this over the stimulus duration to obtain the expected number of strikes in response to moving targets with different stereoscopic disparity, size and vertical disparity. We optimised the parameters of the model so as to bring its predictions into agreement with our empirical data on mean strike rate as a function of stimulus size and disparity. The model proves capable of reproducing the relatively broad tuning to size and narrow tuning to stereoscopic disparity seen in mantis striking behaviour. Although the model has only a single centre-surround receptive field in each eye, it displays qualitatively the same interaction between size and disparity as we observed in real mantids: the preferred size increases as simulated prey distance increases beyond the preferred distance. We show that this occurs because of a stereoscopic “false match” between the leading edge of the stimulus in one eye and its trailing edge in the other; further work will be required to find whether such false matches occur in real mantises. Importantly, the model also displays realistic responses to stimuli with vertical disparity and to pairs of identical stimuli offering a “ghost match”, despite not being fitted to these data. This is the first image-computable model of insect stereopsis, and reproduces key features of both neurophysiology and striking behaviour.

Functional morphology of the raptorial forelegs in Mantispa styriaca (Insecta: Neuroptera)

The insect leg is a multifunctional device, varying tremendously in form and function within Insecta: from a common walking leg, to burrowing, swimming or jumping devices, up to spinning apparatuses or tools for prey capturing. Raptorial forelegs, as predatory striking and grasping devices, represent a prominent example for convergent evolution within insects showing strong morphological and behavioural adaptations for a lifestyle as an ambush predator. However, apart from praying mantises (Mantodea)—the most prominent example of this lifestyle—the knowledge on morphology, anatomy, and the functionality of insect raptorial forelegs, in general, is scarce. Here, we show a detailed morphological description of raptorial forelegs of Mantispa styriaca (Neuroptera), including musculature and the material composition in their cuticle; further, we will discuss the mechanism of the predatory strike. We could confirm all 15 muscles previously described for mantis lacewings, regarding extrinsic and intrinsic musculature, expanding it for one important new muscle—M24c. Combining the information from all of our results, we were able to identify a possible catapult mechanism (latch-mediated spring actuation system) as a driving force of the predatory strike, never proposed for mantis lacewings before. Our results lead to a better understanding of the biomechanical aspects of the predatory strike in Mantispidae. This study further represents a starting point for a comprehensive biomechanical investigation of the convergently evolved raptorial forelegs in insects.

A controllable dual-catapult system inspired by the biomechanics of the dragonfly larvae's predatory strike.

The biomechanics underlying the predatory strike of dragonfly larvae is not yet understood. Dragonfly larvae are aquatic ambush predators, capturing their prey with a strongly modified extensible mouthpart. The current theory of hydraulic pressure being the driving force of the predatory strike can be refuted by our manipulation experiments and reinterpretation of former studies. Here, we report evidence for an independently loaded synchronized dual-catapult system. To power the ballistic movement of a single specialized mouthpart, two independently loaded springs simultaneously release and actuate two separate joints in a kinematic chain. Energy for the movement is stored by straining an elastic structure at each joint and, possibly, the surrounding cuticle, which is preloaded by muscle contraction. As a proof of concept, we developed a bioinspired robotic model resembling the morphology and functional principle of the extensible mouthpart. Understanding the biomechanics of the independently loaded synchronized dual-catapult system found in dragonfly larvae can be used to control the extension direction and, thereby, thrust vector of a power-modulated robotic system.

The strike of the dragonfly larvae.

The predatory strike of dragonfly larvae can inspire the design of fast robotic movement with enhanced control and precision.

Waterborne agrichemicals compromise the anti-predatory behavior of zebrafish.

Due to human activities, there is an increasing presence of agrochemicals residues in water bodies, which could be attributed to an increased use of these chemicals, incorrect disposal of packaging materials, and crop leaching. The effects of these residues on prey-predator relationship of aquatic animals are poorly known. Here, we show that fish acutely exposed to glyphosate, 2,4-D, and methylbenzoate-based agrichemicals have their anti-predatory responses impaired. We exposed zebrafish to sub-lethal concentrations of agrichemicals and evaluated their behavioral reaction against a simulated bird predatory strike. We observed that agrichemical-exposed fish spent more time in a risky area, suggesting that the pesticides interfered with their ability of risk perception. Our results highlight the impairment and environmental consequences of agrochemical residues, which can affect aquatic life and crucial elements for life (food web) such as the prey-predator relationship.

The Effects of Temperature on the Kinematics of Rattlesnake Predatory Strikes in Both Captive and Field Environments

The outcomes of predator–prey interactions between endotherms and ectotherms can be heavily influenced by environmental temperature, owing to the difference in how body temperature affects locomotor performance. However, as elastic energy storage mechanisms can allow ectotherms to maintain high levels of performance at cooler body temperatures, detailed analyses of kinematics are necessary to fully understand how changes in temperature might alter endotherm–ectotherm predator–prey interactions. Viperid snakes are widely distributed ectothermic mesopredators that interact with endotherms both as predator and prey. Although there are numerous studies on the kinematics of viper strikes, surprisingly few have analyzed how this rapid movement is affected by temperature. Here we studied the effects of temperature on the predatory strike performance of rattlesnakes (Crotalus spp.), abundant new world vipers, using both field and captive experimental contexts. We found that the effects of temperature on predatory strike performance are limited, with warmer snakes achieving slightly higher maximum strike acceleration, but similar maximum velocity. Our results suggest that, unlike defensive strikes to predators, rattlesnakes may not attempt to maximize strike speed when attacking prey, and thus the outcomes of predatory strikes may not be heavily influenced by changes in temperature.

Temperature affects susceptibility of intertidal limpets to bird predation.

High temperatures resulting in physiological stress and the reduced ability to resist predation can have life-or-death consequences for an organism. We investigated the effects of temperature on the susceptibility to predation for an ectothermic intertidal mollusc (the owl limpet, Lottia gigantea) and its predator (the black oystercatcher, Haematopus bachmani). The ability of L. gigantea to resist bird predation during low tide is determined by the tenacity of attachment to the rock. We developed a transducer to measure the force of predatory attacks on limpets by a captive black oystercatcher, and tested the hypothesis that exposure to warm temperatures during low tide emersion would affect the limpet's ability to resist dislodgement in trials with a morphometrically accurate beak mimic and a live bird. In beak mimic trials, four times as many limpets exposed to warm low tides were removed, as compared with limpets exposed to cool low tides or in 'no low tide' submerged conditions. Minimum time before limpet removal in captive bird trials was more than six times longer for limpets in cool low tide or no low tide treatments compared with limpets in the warm low tide treatment. We measured shear forces up to 36.63 N during predatory strikes. These direct measurements of the forces exerted by a living oystercatcher provide context for interactions with multiple prey species. Our data suggest that naturally occurring variation in body temperatures among individual prey items in the field could be an important driver of predator-prey interactions and subsequently community patterns.

Neck mobility in the Jurassic plesiosaurCryptoclidus eurymerus: finite element analysis as a new approach to understanding the cervical skeleton in fossil vertebrates

The sauropterygian clade Plesiosauria arose in the Late Triassic and survived to the very end of the Cretaceous. Plesiosauria evolved the greatest species diversity of any marine reptile clade, attaining a global distribution. Plesiosauria consist of two clades, Rhomaleosauridae and Neoplesiosauria. Basal Neoplesiosauria have long necks with at least 30 cervicals, but show qualitative osteological evidence for a stiff neck. Here we quantify neck mobility in lateral, ventral, and dorsal directions based on finite element modeling of neck vertebrae from the Middle Jurassic plesiosaur Cryptoclidus eurymerus. We model the mobility in a single motion segment, consisting of two adjacent cervical vertebrae and the joints connecting them. Based on the model with a maximum intervertebral spacing of 3 mm, we find that in Cryptoclidus, the maximum angle of lateral deflection in the motion segment was 2°. The maximum angle of ventral deflection was 5° and of dorsal deflection was 5°. When these values are multiplied by the number of cervical vertebrae, it becomes apparent that neck mobility was limited in all directions. The maximum angle of total lateral deflection in the neck was 67°. The maximum angle of total ventral deflection was 148° and of total dorsal deflection was 157°. This raises the question of the function of such a long, multi-segment but immobile neck. We posit that the long neck served in hydrodynamic and visual camouflage, hiding the bulk of the body from the small but abundant prey, such as schooling fish and squid. Neck immobility may have been advantageous in withstanding strong hydrodynamic forces acting on the neck during predatory strikes.

Defensive posture in a terrestrial salamander deflects predatory strikes irrespective of body size

Abstract A wide variety of prey use defensive postures as a means of protection from predators. Many salamanders engage in broadly similar defensive postures, which may function as a warning signal and reduce the probability of attack, or may deflect predator attacks away from vital body parts. The extent to which these strategies (i.e., aposematism and deflection) act exclusively or synergistically, however, remains unknown. We deployed clay salamanders in the field, manipulating size (small, large) and posture (resting, defensive), and documented attack rates across three predator types. Competing risks analysis revealed that attack rates were affected by model size, deployment period, and leaf litter depth at the site of deployment, whereas model posture had no significant effect. Model size and posture did not interact, indicating that defensive posture was ineffective in deterring attack irrespective of prey size. Model prey in the defensive posture received significantly more attacks on the tail irrespective of size, and the defensive posture was more effective at deflecting avian attacks compared to mammal predation. We conclude that defensive posture increases tail conspicuousness without increasing predation risk, and primarily functions to deflect attacks away from vital body parts. The efficacy of defection may be further increased by tail undulation, however our use of static models means that we cannot exclude aposematic or deimatic functions for such movements. Our results provide important support for the deflection hypothesis in explaining antipredator behavior, and thereby set the stage for additional research targeting the functionality of attack deflection in natural predator–prey encounters.

External power amplification drives prey capture in a spider web

Power amplification allows animals to produce movements that exceed the physiological limits of muscle power and speed, such as the mantis shrimp's ultrafast predatory strike and the flea's jump. However, all known examples of nonhuman, muscle-driven power amplification involve anatomical structures that store energy from a single cycle of muscular contraction. Here, we describe a nonhuman example of external power amplification using a constructed device: the web of the triangle-weaver spider, Hyptiotes cavatus, which uses energy stored in the silk threads to actively tangle prey from afar. Hyptiotes stretches its web by tightening a separate anchor line over multiple cycles of limb motion, and then releases its hold on the anchor line when insects strike the web. Both spider and web spring forward 2 to 3 cm with a peak acceleration of up to 772.85 m/s2 so that up to four additional adhesive capture threads contact the prey while jerking caused by the spider's sudden stop subsequently wraps silk around the prey from all directions. Using webs as external "tools" to store energy offers substantial mechanical advantages over internal tissue-based power amplification due to the ability of Hyptiotes to load the web over multiple cycles of muscular contraction and thus release more stored energy during prey capture than would be possible with muscle-driven anatomical elastic-energy systems. Elastic power amplification is an underappreciated component of silk's function in webs and shows remarkable convergence to the fundamental mechanical advantages that led humans to engineer power-amplifying devices such as catapults and ballistae.

Motion-in-depth perception and prey capture in the praying mantisSphodromantis lineola

Perceiving motion-in-depth is essential to detecting approaching or receding objects, predators and prey. This can be achieved using several cues, including binocular stereoscopic cues such as changing disparity and interocular velocity differences, and monocular cues such as looming. Although these have been studied in detail in humans, only looming responses have been well characterized in insects and we know nothing about the role of stereoscopic cues and how they might interact with looming cues. We used our 3D insect cinema in a series of experiments to investigate the role of the stereoscopic cues mentioned above, as well as looming, in the perception of motion-in-depth during predatory strikes by the praying mantis Sphodromantis lineola Our results show that motion-in-depth does increase the probability of mantis strikes but only for the classic looming stimulus, an expanding luminance edge. Approach indicated by radial motion of a texture or expansion of a motion-defined edge, or by stereoscopic cues, all failed to elicit increased striking. We conclude that mantises use stereopsis to detect depth but not motion-in-depth, which is detected via looming.

The evolution of anti-bat sensory illusions in moths.

Prey transmit sensory illusions to redirect predatory strikes, creating a discrepancy between what a predator perceives and reality. We use the acoustic arms race between bats and moths to investigate the evolution and function of a sensory illusion. The spinning hindwing tails of silk moths (Saturniidae) divert bat attack by reflecting sonar to create a misleading echoic target. We characterized geometric morphometrics of moth hindwings across silk moths, mapped these traits onto a new, robust phylogeny, and found that elaborated hindwing structures have converged on four adaptive shape peaks. To test the mechanism underlying these anti-bat traits, we pit bats against three species of silk moths with experimentally altered hindwings that created a representative gradient of ancestral and extant hindwing shapes. High-speed videography of battles reveals that moths with longer hindwings and tails more successfully divert bat attack. We postulate that sensory illusions are widespread and are underappreciated drivers of diversity across systems.

Mutualistic cleaner fish maintains high escape performance despite privileged relationship with predators.

Predatory reef fishes regularly visit mutualistic cleaner fish (Labroides dimidiatus) to get their ectoparasites removed but show no interest in eating them. The concept of compensated trait loss posits that characters can be lost if a mutualistic relationship reduces the need for a given trait. Thus, selective pressures on escape performance might have relaxed in L. dimidiatus due to its privileged relationship with predators. However, the cost of failing to escape a predatory strike is extreme even if predation events on cleaners are exceptionally rare. Additionally, cleaners must escape from non-predatory clients that regularly punish them for eating mucus instead of parasites. Therefore, strong escape capabilities might instead be maintained in cleaner fish because they must be able to flee when in close proximity to predators or dissatisfied clients. We compared the fast-start escape performance of L. dimidiatus with that of five closely related wrasse species and found that the mutualistic relationship that cleaners entertain with predators has not led to reduced escape performance. Instead, conflicts in cleaning interactions appear to have maintained selective pressures on this trait, suggesting that compensated trait loss might only evolve in cases of high interdependence between mutualistic partners that are not tempted to cheat.

Observations on the chemosensory responses of the midget faded rattlesnake (Crotalus oreganus concolor): discrimination of envenomated prey in a type II venom species

Rattlesnakes use prey chemical cues for ambush site selection and for relocating envenomated (E) prey following a predatory strike. The ability to discriminate between E and non-envenomated (NE) prey cues has been widely studied in rattlesnake species that produce type I venoms, which show high levels of snake venom metalloproteinase (SVMP) activity and low lethal toxicity [lethal dose which kills 50% of test animals (LD50) >1.0 µg/g]. However, E vs. NE prey discrimination studies have not been conducted on rattlesnake species that produce a type II venom that consists of low SVMP activity and high lethal toxicity (LD50 <1.0 µg/g). In the current study, long-term captive Crotalus oreganus concolor, which produce a type II venom, were tested for their ability to discriminate between chemical cues of natural (Sceloporus undulatus and Peromyscus maniculatus) and non-natural (Hemidactylus frenatus and Mus musculus) prey cues, as well as for their ability to discriminate between E and NE mouse carcasses, when prey envenomation occurred by a conspecific. Snakes showed significant levels of tongue flicking towards the chemical extracts of P. maniculatus and M. musculus, suggesting that C. oreganus concolor exhibit both innate and experience-based plasticity in response to prey chemical cues. In addition, C. oreganus concolor were able to discriminate between E and NE prey sources, when envenomation occurred by a conspecific, indicating that a type II venomous species can also discriminate between E and NE chemical cues.