Not So Fast: Strike Kinematics of the Araneoid Trap-Jaw Spider Pararchaea alba (Malkaridae: Pararchaeinae).

To capture prey otherwise unattainable by muscle function alone, some animal lineages have evolved movements that are driven by stored elastic energy, producing movements of remarkable speed and force. One such example that has evolved multiple times is a trap-jaw mechanism, in which the mouthparts of an animal are loaded with energy as they open to a wide gape and then, when triggered to close, produce a terrific force. Within the spiders (Araneae), this type of attack has thus far solely been documented in the palpimanoid family Mecysmaucheniidae but a similar morphology has also been observed in the distantly related araneoid subfamily Pararchaeinae, leading to speculation of a trap-jaw attack in that lineage as well. Here, using high-speed videography, we test whether cheliceral strike power output suggests elastic-driven movements in the pararchaeine Pararchaea alba. The strike speed attained places P. alba as a moderately fast striker exceeding the slowest mecysmaucheniids, but failing to the reach the most extreme high-speed strikers that have elastic-driven mechanisms. Using microcomputed tomography, we compare the morphology of P. alba chelicerae in the resting and open positions, and their related musculature, and based on results propose a mechanism for cheliceral strike function that includes a torque reversal latching mechanism. Similar to the distantly related trap-jaw mecysmaucheniid spiders, the unusual prosoma morphology in P. alba seemingly allows for highly maneuverable chelicerae with a much wider gape than typical spiders, suggesting that increasingly maneuverable joints coupled with a latching mechanism may serve as a precursor to elastic-driven movements.

The type of leg lost affects habitat use but not survival in a non-regenerating arthropod.

Finding shelter and surviving encounters with predators are pervasive challenges for animals. These challenges may be exacerbated after individuals experience bodily damage. Certain forms of damage arise voluntarily in animals; for instance, some taxa release appendages (tails, legs, or other body parts) as a defensive strategy ("autotomy"). This behavior, however, may pose long-term negative consequences for habitat use and survival. Additionally, these putative consequences are expected to vary according to the function of the lost body part. We tested the effects of losing different functional leg types (locomotor or sensory) on future habitat use and survival in a Neotropical species of Prionostemma harvestmen (Arachnida: Opiliones) that undergo frequent autotomy but do not regrow limbs. Daytime surveys revealed that both eight-legged harvestmen and harvestmen missing legs roosted in similar frequencies across habitats (tree bark, mossy tree, or fern), and perched at similar heights. Mark-recapture data showed that harvestmen that lost sensory legs roosted in tree bark less frequently, but on mossy trees more frequently. On the contrary, we did not observe changes in habitat use for eight-legged animals or animals that lost locomotor legs. This change might be related to sensory exploration and navigation. Lastly, we found that recapture rates across substrates were not affected by the type of legs lost, suggesting that leg loss does not impact survival. This potential lack of effect might play a role in why a defensive strategy like autotomy is so prevalent in harvestmen despite the lack of regeneration.

Jump takeoff in a small jumping spider.

Jumping in animals presents an interesting locomotory strategy as it requires the generation of large forces and accurate timing. Jumping in arachnids is further complicated by their semi-hydraulic locomotion system. Among arachnids, jumping spiders (Family Salticidae) are agile and dexterous jumpers. However, less is known about jumping in small salticid species. Here we used Habronattus conjunctus, a small jumping spider (body length ~ 4.5 mm) to examine its jumping performance and compare it to that of other jumping spiders and insects. We also explored how legs are used during the takeoff phase of jumps. Jumps were staged between two raised platforms. We analyzed jumping videos with DeepLabCut to track 21 points on the cephalothorax, abdomen, and legs. By analyzing leg liftoff and extension patterns, we found evidence that H. conjunctus primarily uses the third legs to power jumps. We also found that H. conjunctus jumps achieve lower takeoff speeds and accelerations than most other jumping arthropods, including other jumping spiders. Habronattus conjunctus takeoff time was similar to other jumping arthropods of the same body mass. We discuss the mechanical benefits and drawbacks of a semi-hydraulic system of locomotion and consider how small spiders may extract dexterous jumps from this locomotor system.

Evolutionary novelty in communication between the sexes.

The diversity of signalling traits within and across taxa is vast and striking, prompting us to consider how novelty evolves in the context of animal communication. Sexual selection contributes to diversification, and here we endeavour to understand the initial conditions that facilitate the maintenance or elimination of new sexual signals and receiver features. New sender and receiver variants can occur through mutation, plasticity, hybridization and cultural innovation, and the initial conditions of the sender, the receiver and the environment then dictate whether a novel cue becomes a signal. New features may arise in the sender, the receiver or both simultaneously. We contend that it may be easier than assumed to evolve new sexual signals because sexual signals may be arbitrary, sexual conflict is common and receivers are capable of perceiving much more of the world than just existing sexual signals. Additionally, changes in the signalling environment can approximate both signal and receiver changes through a change in transmission characteristics of a given environment or the use of new environments. The Anthropocene has led to wide-scale disruption of the environment and may thus generate opportunity to directly observe the evolution of new signals to address questions that are beyond the reach of phylogenetic approaches.

Leg loss decreases endurance and increases oxygen consumption during locomotion in harvestmen.

Animal movements are highly constrained by morphology and energetics. In addition, predictable bodily damage can constrain locomotion even further. For example, for animals moving on land, losing legs may impose additional costs. We tested if losing legs affects the distance travelled over time (endurance) and the metabolic costs of locomotion (oxygen consumption) in Nelima paessleri harvestmen. These arachnids voluntary releases legs (i.e., autotomy) in response to predation attempts. We used flow-through respirometry as animals moved on a treadmill inside a sealed chamber. We found that endurance decreased gradually with an increasing number of legs lost. Interestingly, oxygen consumption increased only for harvestmen that lost three legs, but not for individuals that lost only a single leg. These results have different ecological and evolutionary implications. Reduced endurance may impair an animal's ability to continue moving away from potential predators, while increased oxygen consumption makes movement costlier. Our findings suggest that individuals have a threshold number of legs that can be lost before experiencing measurable energetic consequences. Overall, our findings illustrate how animals respond to morphological modifications (i.e., damage) that affect the physiology of locomotion.

Rapid recovery of locomotor performance after leg loss in harvestmen.

Animals have evolved adaptations to deal with environmental challenges. For instance, voluntarily releasing appendages (autotomy) to escape potential predators. Although it may enhance immediate survival, this self-imposed bodily damage may convey long-term consequences. Hence, compensatory strategies for this type of damage might exist. We experimentally induced autotomy in Prionostemma harvestmen. These arachnids are ideal to examine this topic because they show high levels of leg loss in the field but do not regenerate their legs. We video-recorded animals moving on a horizontal track and reconstructed their 3D trajectories with custom software tools to measure locomotor performance. Individuals that lost either three legs total or two legs on the same side of the body showed an immediate and substantial decrease in velocity and acceleration. Surprisingly, harvestmen recovered initial performance after 2 days. This is the quickest locomotor recovery recorded for autotomizing animals. We also found post-autotomy changes in stride and postural kinematics, suggesting a role for kinematic adjustments in recovery. Additionally, following leg loss, some animals changed the gaits used during escape maneuvers, and/or recruited the 'sensory' legs for locomotion. Together, these findings suggest that harvestmen are mechanically robust to the bodily damage imposed by leg loss.

Low temperatures impact species distributions of jumping spiders across a desert elevational cline.

Temperature is known to influence many aspects of organisms and is frequently linked to geographical species distributions. Despite the importance of a broad understanding of an animal's thermal biology, few studies incorporate more than one metric of thermal biology. Here we examined an elevational assemblage of Habronattus jumping spiders to measure different aspects of their thermal biology including thermal limits (CTmin, CTmax), thermal preference, V̇CO2 as proxy for metabolic rate, locomotor behavior and warming tolerance. We used these data to test whether thermal biology helped explain how species were distributed across elevation. Habronattus had high CTmax values, which did not differ among species across the elevational gradient. The highest-elevation species had a lower CTmin than any other species. All species had a strong thermal preference around 37 °C. With respect to performance, one of the middle elevation species was significantly less temperature-sensitive in metabolic rate. Differences between species with respect to locomotion (jump distance) were likely driven by differences in mass, with no differences in thermal performance across elevation. We suggest that Habronattus distributions follow Brett's rule, a rule that predicts more geographical variation in cold tolerance than heat. Additionally, we suggest that physiological tolerances interact with biotic factors, particularly those related to courtship and mate choice to influence species distributions. Habronattus also had very high warming tolerance values (> 20 °C, on average). Taken together, these data suggest that Habronattus are resilient in the face of climate-change related shifts in temperature.

Growling from the gut: co-option of the gastric mill for acoustic communication in ghost crabs.

Animal acoustic communication systems can be built upon co-opted structures that become specialized for sound production or morphological novelties. The ghost crab, Ocypode quadrata, evolved a novel stridulation apparatus on the claws that is used during agonistic interactions, but they also produce a rasping sound without their claw apparatus. We investigated the nature of these sounds and show that O. quadrata adopted a unique and redundant mode of sound production by co-opting the gastric mill (grinding teeth of the foregut). Acoustic characteristics of the sound are consistent with stridulation and are produced by both male and female crabs during aggressive interactions. Laser Doppler vibrometry localized the source of maximum vibration to the gastric region and fluoroscopy showed movement of the gastric mill that coincided with stridulation. The lateral teeth of the gastric mill possess a series of comb-like structures that rub against the median tooth to produce stridulation with dominant frequencies below 2 kHz. This previously undescribed gastric stridulation can be modulated and provide a means of assessment during aggressive interactions, similar to the use of the claw stridulation apparatus. This functional redundancy of stridulation in crabs offers unique insights into the mechanisms of evolution of acoustic communication systems.

Nonlinear changes in selection on a mating display across a continuous thermal gradient.

Understanding how animal communication varies across time and space is critical to understanding how animal signals have evolved and how they function. Changes in temperature, which occur across both time and space, can alter both the courtship and mate choice behaviour of ectothermic animals. In this study, we examine the effect of daily thermal variation on courtship and mate choice in the wolf spider Schizocosa floridana, which produces a complex song with vibrations from three distinct body parts. We test the hypothesis that different components of S. floridana's courtship respond differently to daily changes in temperature and that corresponding mate choice patterns lead to complex, overlapping shifts in selection on the display itself. By manipulating the thermal environment of courting and choosing pairs, we found that several song components increased in production rate with increased temperature, whereas others decreased, or did not respond at all. We also found evidence that selection on courtship shifts with temperature in several ways, with some display components experiencing directional selection at higher temperatures, but not at lower temperatures. Our findings make it clear that understanding the effect of environmental variation on communication is critical to understanding how selection operates on mate choice and how signals, particularly complex signals, evolve.

Anthropogenic noise and the bioacoustics of terrestrial invertebrates.

Anthropogenic noise is an important issue of environmental concern owing to its wide-ranging effects on the physiology, behavior and ecology of animals. To date, research has focused on the impacts of far-field airborne noise (i.e. pressure waves) on vertebrates, with few exceptions. However, invertebrates and the other acoustic modalities they rely on, primarily near-field airborne and substrate-borne sound (i.e. particle motion and vibrations, respectively) have received little attention. Here, we review the literature on the impacts of different types of anthropogenic noise (airborne far-field, airborne near-field, substrate-borne) on terrestrial invertebrates. Using literature on invertebrate bioacoustics, we propose a framework for understanding the potential impact of anthropogenic noise on invertebrates and outline predictions of possible constraints and adaptations for invertebrates in responding to anthropogenic noise. We argue that understanding the impacts of anthropogenic noise requires us to consider multiple modalities of sound and to cultivate a broader understanding of invertebrate bioacoustics.

The return to water in ancestral Xenopus was accompanied by a novel mechanism for producing and shaping vocal signals.

Listeners locate potential mates using species-specific vocal signals. As tetrapods transitioned from water to land, lungs replaced gills, allowing expiration to drive sound production. Some frogs then returned to water. Here we explore how air-driven sound production changed upon re-entry to preserve essential acoustic information on species identity in the secondarily aquatic frog genus Xenopus. We filmed movements of cartilage and muscles during evoked sound production in isolated larynges. Results refute the current theory for Xenopus vocalization, cavitation, and favor instead sound production by mechanical excitation of laryngeal resonance modes following rapid separation of laryngeal arytenoid discs. Resulting frequency resonance modes (dyads) are intrinsic to the larynx rather than due to neuromuscular control. Dyads are a distinctive acoustic signature. While their component frequencies overlap across species, their ratio is shared within each Xenopus clade providing information on species identity that could facilitate both conspecific localization and ancient species divergence. Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter).

Resonance frequencies of honeybee (Apis mellifera) wings.

During flight, insect wings bend and twist under the influence of aerodynamic and inertial forces. We tested whether wing resonance of honeybees (Apis mellifera) matches the wingbeat frequency, against the 'stiff element' hypothesis that the wing's first longitudinal mode exceeds the wingbeat frequency. Six bees were immobilized with their right wing pair outspread, and stimulated with a shaker while the normal modes were recorded with a scanning Doppler laser vibrometer. The lowest normal mode of the wings was the first longitudinal bending mode and, at 602±145 Hz, was greater than the wingbeat frequency of 234±13.9 Hz. Higher-order normal modes of the wing tended to incorporate nodal lines in the chordwise direction of the trailing edge, suggesting that their mode shape did not strongly resemble wing deformation during flapping flight. These results support the stiff element hypothesis for Apis mellifera.

Airborne Acoustic Perception by a Jumping Spider.

Jumping spiders (Salticidae) are famous for their visually driven behaviors [1]. Here, however, we present behavioral and neurophysiological evidence that these animals also perceive and respond to airborne acoustic stimuli, even when the distance between the animal and the sound source is relatively large (∼3 m) and with stimulus amplitudes at the position of the spider of ∼65 dB sound pressure level (SPL). Behavioral experiments with the jumping spider Phidippus audax reveal that these animals respond to low-frequency sounds (80 Hz; 65 dB SPL) by freezing-a common anti-predatory behavior characteristic of an acoustic startle response. Neurophysiological recordings from auditory-sensitive neural units in the brains of these jumping spiders showed responses to low-frequency tones (80 Hz at ∼65 dB SPL)-recordings that also represent the first record of acoustically responsive neural units in the jumping spider brain. Responses persisted even when the distances between spider and stimulus source exceeded 3 m and under anechoic conditions. Thus, these spiders appear able to detect airborne sound at distances in the acoustic far-field region, beyond the near-field range often thought to bound acoustic perception in arthropods that lack tympanic ears (e.g., spiders) [2]. Furthermore, direct mechanical stimulation of hairs on the patella of the foreleg was sufficient to generate responses in neural units that also responded to airborne acoustic stimuli-evidence that these hairs likely play a role in the detection of acoustic cues. We suggest that these auditory responses enable the detection of predators and facilitate an acoustic startle response. VIDEO ABSTRACT.

Repeated Evolution of Power-Amplified Predatory Strikes in Trap-Jaw Spiders.

Small animals possess intriguing morphological and behavioral traits that allow them to capture prey, including innovative structural mechanisms that produce ballistic movements by amplifying power [1-6]. Power amplification occurs when an organism produces a relatively high power output by releasing slowly stored energy almost instantaneously, resulting in movements that surpass the maximal power output of muscles [7]. For example, trap-jaw, power-amplified mechanisms have been described for several ant genera [5, 8], which have evolved some of the fastest known movements in the animal kingdom [6]. However, power-amplified predatory strikes were not previously known in one of the largest animal classes, the arachnids. Mecysmaucheniidae spiders, which occur only in New Zealand and southern South America, are tiny, cryptic, ground-dwelling spiders that rely on hunting rather than web-building to capture prey [9]. Analysis of high-speed video revealed that power-amplified mechanisms occur in some mecysmaucheniid species, with the fastest species being two orders of magnitude faster than the slowest species. Molecular phylogenetic analysis revealed that power-amplified cheliceral strikes have evolved four times independently within the family. Furthermore, we identified morphological innovations that directly relate to cheliceral function: a highly modified carapace in which the cheliceral muscles are oriented horizontally; modification of a cheliceral sclerite to have muscle attachments; and, in the power-amplified species, a thicker clypeus and clypeal apodemes. These structural innovations may have set the stage for the parallel evolution of ballistic predatory strikes.

Female preference for multi-modal courtship: multiple signals are important for male mating success in peacock spiders.

A long-standing goal for biologists has been to understand how female preferences operate in systems where males have evolved numerous sexually selected traits. Jumping spiders of the Maratus genus are exceptionally sexually dimorphic in appearance and signalling behaviour. Presumably, strong sexual selection by females has played an important role in the evolution of complex signals displayed by males of this group; however, this has not yet been demonstrated. In fact, despite apparent widespread examples of sexual selection in nature, empirical evidence is relatively sparse, especially for species employing multiple modalities for intersexual communication. In order to elucidate whether female preference can explain the evolution of multi-modal signalling traits, we ran a series of mating trials using Maratus volans. We used video recordings and laser vibrometry to characterize, quantify and examine which male courtship traits predict various metrics of mating success. We found evidence for strong sexual selection on males in this system, with success contingent upon a combination of visual and vibratory displays. Additionally, independently produced, yet correlated suites of multi-modal male signals are linked to other aspects of female peacock spider behaviour. Lastly, our data provide some support for both the redundant signal and multiple messages hypotheses for the evolution of multi-modal signalling.

Hummingbird feather sounds are produced by aeroelastic flutter, not vortex-induced vibration.

Males in the 'bee' hummingbird clade produce distinctive, species-specific sounds with fluttering tail feathers during courtship displays. Flutter may be the result of vortex shedding or aeroelastic interactions. We investigated the underlying mechanics of flutter and sound production of a series of different feathers in a wind tunnel. All feathers tested were capable of fluttering at frequencies varying from 0.3 to 10 kHz. At low airspeeds (Uair) feather flutter was highly damped, but at a threshold airspeed (U*) the feathers abruptly entered a limit-cycle vibration and produced sound. Loudness increased with airspeed in most but not all feathers. Reduced frequency of flutter varied by an order of magnitude, and declined with increasing Uair in all feathers. This, along with the presence of strong harmonics, multiple modes of flutter and several other non-linear effects indicates that flutter is not simply a vortex-induced vibration, and that the accompanying sounds are not vortex whistles. Flutter is instead aeroelastic, in which structural (inertial/elastic) properties of the feather interact variably with aerodynamic forces, producing diverse acoustic results.

Structural resonance and mode of flutter of hummingbird tail feathers.

Feathers can produce sound by fluttering in airflow. This flutter is hypothesized to be aeroelastic, arising from the coupling of aerodynamic forces to one or more of the feather's intrinsic structural resonance frequencies. We investigated how mode of flutter varied among a sample of hummingbird tail feathers tested in a wind tunnel. Feather vibration was measured directly at ~100 points across the surface of the feather with a scanning laser Doppler vibrometer (SLDV), as a function of airspeed, Uair. Most feathers exhibited multiple discrete modes of flutter, which we classified into types including tip, trailing vane and torsional modes. Vibratory behavior within a given mode was usually stable, but changes in independent variables such as airspeed or orientation sometimes caused feathers to abruptly 'jump' from one mode to another. We measured structural resonance frequencies and mode shapes directly by measuring the free response of 64 feathers stimulated with a shaker and recorded with the SLDV. As predicted by the aeroelastic flutter hypothesis, the mode shape (spatial distribution) of flutter corresponded to a bending or torsional structural resonance frequency of the feather. However, the match between structural resonance mode and flutter mode was better for tip or torsional mode shapes, and poorer for trailing vane modes. Often, the 3rd bending structural harmonic matched the expressed mode of flutter, rather than the fundamental. We conclude that flutter occurs when airflow excites one or more structural resonance frequencies of a feather, most akin to a vibrating violin string.

The effect of surface wave propagation on neural responses to vibration in primate glabrous skin.

Because tactile perception relies on the response of large populations of receptors distributed across the skin, we seek to characterize how a mechanical deformation of the skin at one location affects the skin at another. To this end, we introduce a novel non-contact method to characterize the surface waves produced in the skin under a variety of stimulation conditions. Specifically, we deliver vibrations to the fingertip using a vibratory actuator and measure, using a laser Doppler vibrometer, the surface waves at different distances from the locus of stimulation. First, we show that a vibration applied to the fingertip travels at least the length of the finger and that the rate at which it decays is dependent on stimulus frequency. Furthermore, the resonant frequency of the skin matches the frequency at which a subpopulation of afferents, namely Pacinian afferents, is most sensitive. We show that this skin resonance can lead to a two-fold increase in the strength of the response of a simulated afferent population. Second, the rate at which vibrations propagate across the skin is dependent on the stimulus frequency and plateaus at 7 m/s. The resulting delay in neural activation across locations does not substantially blur the temporal patterning in simulated populations of afferents for frequencies less than 200 Hz, which has important implications about how vibratory frequency is encoded in the responses of somatosensory neurons. Third, we show that, despite the dependence of decay rate and propagation speed on frequency, the waveform of a complex vibration is well preserved as it travels across the skin. Our results suggest, then, that the propagation of surface waves promotes the encoding of spectrally complex vibrations as the entire neural population is exposed to essentially the same stimulus. We also discuss the implications of our results for biomechanical models of the skin.

Multi-modal courtship in the peacock spider, Maratus volans (O.P.-Cambridge, 1874).

The peacock spider, Maratus volans, has one of the most elaborate courtship displays in arthropods. Using regular and high-speed video segments captured in the lab, we provide detailed descriptions of complete male courtship dances. As research on jumping spiders has demonstrated that males of some species produce vibrations concurrently with visual displays, we also used laser vibrometry to uncover such elements for this species. Our recordings reveal and describe for the first time, that M. volans males use vibratory signals in addition to complex body ornaments and motion displays. The peacock spider and other closely related species are outstanding study organisms for testing hypotheses about the evolution and functional significance of complex displays, thus, this descriptive study establishes a new model system for behavioral ecology, one that certainly stands to make important contributions to the field.

Aeroelastic flutter produces hummingbird feather songs.

During courtship flights, males of some hummingbird species produce diverse sounds with tail feathers of varying shapes. We show that these sounds are produced by air flowing past a feather, causing it to aeroelastically flutter and generate flutter-induced sound. Scanning laser doppler vibrometery and high-speed video of individual feathers of different sizes and shapes in a wind tunnel revealed multiple vibratory modes that produce a range of acoustic frequencies and harmonic structures. Neighboring feathers can be aerodynamically coupled and flutter either at the same frequency, resulting in sympathetic vibrations that increase loudness, or at different frequencies, resulting in audible interaction frequencies. Aeroelastic flutter is intrinsic to stiff airfoils such as feathers and thus explains tonal sounds that are common in bird flight.