Eye-specific detection and a multi-eye integration model of biological motion perception.

'Biological motion' refers to the distinctive kinematics observed in many living organisms, where visually perceivable points on the animal move at fixed distances from each other. Across the animal kingdom, many species have developed specialized visual circuitry to recognize such biological motion and to discriminate it from other patterns. Recently, this ability has been observed in the distributed visual system of jumping spiders. These eight-eyed animals use six eyes to perceive motion, while the remaining two (the principal anterior medial eyes) are shifted across the visual scene to further inspect detected objects. When presented with a biologically moving stimulus and a random one, jumping spiders turn to face the latter, clearly demonstrating the ability to discriminate between them. However, it remains unclear whether the principal eyes are necessary for this behavior, whether all secondary eyes can perform this discrimination, or whether a single eye-pair is specialized for this task. Here, we systematically tested the ability of jumping spiders to discriminate between biological and random visual stimuli by testing each eye-pair alone. Spiders were able to discriminate stimuli only when the anterior lateral eyes were unblocked, and performed at chance levels in other configurations. Interestingly, spiders showed a preference for biological motion over random stimuli - unlike in past work. We therefore propose a new model describing how specialization of the anterior lateral eyes for detecting biological motion contributes to multi-eye integration in this system. This integration generates more complex behavior through the combination of simple, single-eye responses. We posit that this in-built modularity may be a solution to the limited resources of these invertebrates' brains, constituting a novel approach to visual processing.

The evolution and ecology of multiple antipredator defences.

Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such "defence portfolios" that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.

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.

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.

Author Correction: Sole coloration as an unusual aposematic signal in a Neotropical toad.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Sexual Dichromatism Drives Diversification within a Major Radiation of African Amphibians.

Theory predicts that sexually dimorphic traits under strong sexual selection, particularly those involved with intersexual signaling, can accelerate speciation and produce bursts of diversification. Sexual dichromatism (sexual dimorphism in color) is widely used as a proxy for sexual selection and is associated with rapid diversification in several animal groups, yet studies using phylogenetic comparative methods to explicitly test for an association between sexual dichromatism and diversification have produced conflicting results. Sexual dichromatism is rare in frogs, but it is both striking and prevalent in African reed frogs, a major component of the diverse frog radiation termed Afrobatrachia. In contrast to most other vertebrates, reed frogs display female-biased dichromatism in which females undergo color transformation, often resulting in more ornate coloration in females than in males. We produce a robust phylogeny of Afrobatrachia to investigate the evolutionary origins of sexual dichromatism in this radiation and examine whether the presence of dichromatism is associated with increased rates of net diversification. We find that sexual dichromatism evolved once within hyperoliids and was followed by numerous independent reversals to monochromatism. We detect significant diversification rate heterogeneity in Afrobatrachia and find that sexually dichromatic lineages have double the average net diversification rate of monochromatic lineages. By conducting trait simulations on our empirical phylogeny, we demonstrate that our inference of trait-dependent diversification is robust. Although sexual dichromatism in hyperoliid frogs is linked to their rapid diversification and supports macroevolutionary predictions of speciation by sexual selection, the function of dichromatism in reed frogs remains unclear. We propose that reed frogs are a compelling system for studying the roles of natural and sexual selection on the evolution of sexual dichromatism across micro- and macroevolutionary timescales.

Sole coloration as an unusual aposematic signal in a Neotropical toad.

Many animals have evolved remarkable strategies to avoid predation. In diurnal, toxic harlequin toads (Atelopus) from the Amazon basin, we find a unique colour signal. Some Atelopus populations have striking red soles of the hands and feet, visible only when walking. When stationary, the toads are hard to detect despite their yellow-black dorsal coloration. Consequently, they switch between high and low conspicuousness. Interestingly, some populations lack the extra colour display of the soles. We found comprehensive support that the red coloration can act as an aposematic signal directed towards potential predators: red soles are significantly more conspicuous than soles lacking red coloration to avian predators and the presence of the red signal significantly increases detection. Further, toads with red soles show bolder behaviour by using higher sites in the vegetation than those lacking this signal. Field experiments hint at a lower attack risk for clay models with red soles than for those lacking the signal, in a population where the red soles naturally occur. We suggest that the absence of the signal may be explained by a higher overall attack risk or potential differences of predator community structure between populations.

Geographic range expansion of tetrodotoxin in amphibians - First record in Atelopus hoogmoedi from the Guiana Shield.

For the first time, alcohol extracts of Atelopus hoogmoedi from the Guiana Shield in Suriname and Guyana were analyzed for the presence of tetrodotoxin (TTX) and of its analogues by high resolution hydrophilic interaction liquid chromatography/mass spectrometry. One specimen from Suriname was found to contain TTX and 4-epiTTX. Using a monoclonal antibody-based immunohistochemical staining technique, TTX was localized mainly in the granular glands and epithelium of the skin, but not in internal organs except liver showing weak TTX-positive reaction. In two specimens collected in Guyana, none of the toxins were detected.

Tetrodotoxin.

In this Quick Guide, Lorentz et al. discuss the function of tetrodotoxin and its distribution in the animal kingdom.

Do poison frogs recognize chemical cues of the other sex or do they react to cues of stressed conspecifics?

Although anuran communication primarily takes place acoustically, chemical cues are also often used for intra- and intersexual communication in frogs. In the present study we analyzed the behavior of the poison frog Ranitomeya variabilis when presented chemical cues of same-sex or opposite-sex conspecifics. Chemical cues were obtained by keeping a single frog on a moist paper towel for about 47h. Afterwards two paper towels were offered to a test animal, one containing the chemical cues, the other containing rainwater only. We ran trials presenting female cues to males, males cues to males as well as male cues to females. The results of the trials were not significant in terms of intersexual communication. The overall response revealed a clear avoidance strategy which leads us to the assumption that disturbance cues unintentionally occurred during the experiment. The rather small size of the containers used to obtain chemical cues prior to the trials probably lead to confinement stress which consequently caused increased urination containing stress hormones that were detected by the test animals. This is the first proof of disturbance cues and their effects in adult anurans. The results of this study do not allow conclusions about inter- or intrasexual chemical communication of R. variabilis, but they allow implications and revisions for future experiments on this topic.