Regularly occurring bouts of retinal movements suggest an REM sleep-like state in jumping spiders.

Sleep and sleep-like states are present across the animal kingdom, with recent studies convincingly demonstrating sleep-like states in arthropods, nematodes, and even cnidarians. However, the existence of different sleep phases across taxa is as yet unclear. In particular, the study of rapid eye movement (REM) sleep is still largely centered on terrestrial vertebrates, particularly mammals and birds. The most salient indicator of REM sleep is the movement of eyes during this phase. Movable eyes, however, have evolved only in a limited number of lineages-an adaptation notably absent in insects and most terrestrial arthropods-restricting cross-species comparisons. Jumping spiders, however, possess movable retinal tubes to redirect gaze, and in newly emerged spiderlings, these movements can be directly observed through their temporarily translucent exoskeleton. Here, we report evidence for an REM sleep-like state in a terrestrial invertebrate: periodic bouts of retinal movements coupled with limb twitching and stereotyped leg curling behaviors during nocturnal resting in a jumping spider. Observed retinal movement bouts were consistent, including regular durations and intervals, with both increasing over the course of the night. That these characteristic REM sleep-like behaviors exist in a highly visual, long-diverged lineage further challenges our understanding of this sleep state. Comparisons across such long-diverged lineages likely hold important questions and answers about the visual brain as well as the origin, evolution, and function of REM sleep.

Rapid mid-jump production of high-performance silk by jumping spiders.

Jumping spiders (Salticidae) do not rely on webs to capture their prey, but they do spin a silk dragline behind them as they move through their habitat. They also spin this dragline during jumps, continuously connecting them with the surface they leapt from. Because spiders cannot spin silk in advance, this silk must be spun at the same speed as the spider jumps - in effect, requiring spin speeds over ten times faster than typical. And while many spiders can move rapidly, for example when running or rappelling, previous research on silk has found that silk spinning rates in excess of walking and web-building speeds (∼2-20 mm/s) result in lower quality silk and even dragline failure1. Here we report that, despite being spun at high speeds (∼500-700 mm/s; 100-140 body lengths/s), jump-spun salticid silk shows consistent, uniform structure as well as the high-performance qualities characteristic of silk spun by other spiders, including orb-weaving species, at low speeds2. The toughness of this jump-spun silk (mean = 281.9 MJ/m3) even surpasses reported values for all but the toughest orb-web draglines2. These results show that salticids are capable of spinning high-performance silk and are able to do so extremely rapidly under natural conditions.

Perception of biological motion by jumping spiders.

The body of most creatures is composed of interconnected joints. During motion, the spatial location of these joints changes, but they must maintain their distances to one another, effectively moving semirigidly. This pattern, termed "biological motion" in the literature, can be used as a visual cue, enabling many animals (including humans) to distinguish animate from inanimate objects. Crucially, even artificially created scrambled stimuli, with no recognizable structure but that maintains semirigid movement patterns, are perceived as animated. However, to date, biological motion perception has only been reported in vertebrates. Due to their highly developed visual system and complex visual behaviors, we investigated the capability of jumping spiders to discriminate biological from nonbiological motion using point-light display stimuli. These kinds of stimuli maintain motion information while being devoid of structure. By constraining spiders on a spherical treadmill, we simultaneously presented 2 point-light displays with specific dynamic traits and registered their preference by observing which pattern they turned toward. Spiders clearly demonstrated the ability to discriminate between biological motion and random stimuli, but curiously turned preferentially toward the latter. However, they showed no preference between biological and scrambled displays, results that match responses produced by vertebrates. Crucially, spiders turned toward the stimuli when these were only visible by the lateral eyes, evidence that this task may be eye specific. This represents the first demonstration of biological motion recognition in an invertebrate, posing crucial questions about the evolutionary history of this ability and complex visual processing in nonvertebrate systems.

Hanging by a thread: unusual nocturnal resting behaviour in a jumping spider.

BACKGROUND: For diurnal animals that heavily rely on vision, a nocturnal resting strategy that offers protection when vision is compromised, is crucial. We found a population of a common European jumping spider (Evarcha arcuata) that rests at night by suspending themselves from a single silk thread attached overhead to the vegetation, a strategy categorically unlike typical retreat-based resting in this group. RESULTS: In a comprehensive study, we collected the first quantitative field and qualitative observation data of this surprising behaviour and provide a detailed description. We tested aspects of site fidelity and disturbance response in the field to assess potential functions of suspended resting. Spiders of both sexes and all developmental stages engage in this nocturnal resting strategy. Interestingly, individual spiders are equally able to build typical silk retreats and thus actively choose between different strategies inviting questions about what factors underlie this behavioural choice. CONCLUSIONS: Our preliminary data hint at a potential sensory switch from visual sensing during the day to silk-borne vibration sensing at night when vision is compromised. The described behaviour potentially is an effective anti-predator strategy either by acting as an early alarm system via vibration sensing or by bringing the animal out of reach for nocturnal predators. We propose tractable hypotheses to test an adaptive function of suspended resting. Further studies will shed light on the sensory challenges that animals face during resting phases and should target the mechanisms and strategies by which such challenges are overcome.

The Long and Short of Hearing in the Mosquito Aedes aegypti.

Mating behavior in Aedes aegypti mosquitoes occurs mid-air and involves the exchange of auditory signals at close range (millimeters to centimeters) [1-6]. It is widely assumed that this intimate signaling distance reflects short-range auditory sensitivity of their antennal hearing organs to faint flight tones [7, 8]. To the contrary, we show here that male mosquitoes can hear the female's flight tone at surprisingly long distances-from several meters to up to 10 m-and that unrestrained, resting Ae. aegypti males leap off their perches and take flight when they hear female flight tones. Moreover, auditory sensitivity tests of Ae. aegypti's hearing organ, made from neurophysiological recordings of the auditory nerve in response to pure-tone stimuli played from a loudspeaker, support the behavioral experiments. This demonstration of long-range hearing in mosquitoes overturns the common assumption that the thread-like antennal hearing organs of tiny insects are strictly close-range ears. The effective range of a hearing organ depends ultimately on its sensitivity [9-13]. Here, a mosquito's antennal ear is shown to be sensitive to sound levels down to 31 dB sound pressure level (SPL), translating to air particle velocity at nanometer dimensions. We note that the peak of energy of the first formant of the vowels of the human speech spectrum range from about 200-1,000 Hz and is typically spoken at 45-70 dB SPL; together, they lie in the sweet spot of mosquito hearing. VIDEO ABSTRACT.

Limping following limb loss increases locomotor stability.

Although many arthropods have the ability to voluntarily lose limbs, how these animals rapidly adapt to such an extreme perturbation remains poorly understood. It is thought that moving with certain gaits can enable efficient, stable locomotion; however, switching gaits requires complex information flow between and coordination of an animal's limbs. We show here that upon losing two legs, spiders can switch to a novel, more statically stable gait, or use temporal adjustments without a gait change. The resulting gaits have higher overall static stability than the gaits that would be imposed by limb loss. By decreasing the time spent in a low-stability configuration - effectively 'limping' over less-stable phases of the stride - spiders increased the overall stability of the less statically stable gait with no observable reduction in speed, as compared with the intact condition. Our results shed light on how voluntary limb loss could have persisted evolutionarily among many animals, and provide bioinspired solutions for robots when they break or lose limbs.

Walking like an ant: a quantitative and experimental approach to understanding locomotor mimicry in the jumping spider Myrmarachne formicaria.

Protective mimicry, in which a palatable species avoids predation by being mistaken for an unpalatable model, is a remarkable example of adaptive evolution. These complex interactions between mimics, models and predators can explain similarities between organisms beyond the often-mechanistic constraints typically invoked in studies of convergent evolution. However, quantitative studies of protective mimicry typically focus on static traits (e.g. colour and shape) rather than on dynamic traits like locomotion. Here, we use high-speed cameras and behavioural experiments to investigate the role of locomotor behaviour in mimicry by the ant-mimicking jumping spider Myrmarachne formicaria, comparing its movement to that of ants and non-mimicking spiders. Contrary to previous suggestions, we find mimics walk using all eight legs, raising their forelegs like ant antennae only when stationary. Mimics exhibited winding trajectories (typical wavelength = 5-10 body lengths), which resemble the winding patterns of ants specifically engaged in pheromone-trail following, although mimics walked on chemically inert surfaces. Mimics also make characteristically short (approx. 100 ms) pauses. Our analysis suggests that this makes mimics appear ant-like to observers with slow visual systems. Finally, behavioural experiments with predatory spiders yield results consistent with the protective mimicry hypothesis. These findings highlight the importance of dynamic behaviours and observer perception in mimicry.

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.

Visual perception in the brain of a jumping spider.

Jumping spiders (Salticidae) are renowned for a behavioral repertoire that can seem more vertebrate, or even mammalian, than spider-like in character. This is made possible by a unique visual system that supports their stalking hunting style and elaborate mating rituals in which the bizarrely marked and colored appendages of males highlight their song-and-dance displays. Salticids perform these tasks with information from four pairs of functionally specialized eyes, providing a near 360° field of view and forward-looking spatial resolution surpassing that of all insects and even some mammals, processed by a brain roughly the size of a poppy seed. Salticid behavior, evolution, and ecology are well documented, but attempts to study the neurophysiological basis of their behavior had been thwarted by the pressurized nature of their internal body fluids, making typical physiological techniques infeasible and restricting all previous neural work in salticids to a few recordings from the eyes. We report the first survey of neurophysiological recordings from the brain of a jumping spider, Phidippus audax (Salticidae). The data include single-unit recordings in response to artificial and naturalistic visual stimuli. The salticid visual system is unique in that high-acuity and motion vision are processed by different pairs of eyes. We found nonlinear interactions between the principal and secondary eyes, which can be inferred from the emergence of spatiotemporal receptive fields. Ecologically relevant images, including prey-like objects such as flies, elicited bursts of excitation from single units.