Saccadic tracking of targets mediated by the anterior-lateral eyes of jumping spiders

The modular visual system of jumping spiders (Salticidae) divides characteristics such as high spatial acuity and wide-field motion detection between different pairs of eyes. A large pair of telescope-like anterior-median (AM) eyes is supported by 2-3 pairs of 'secondary' eyes, which provide almost 360 degrees of visual coverage at lower resolution. The AM retinae are moveable and can be pointed at stimuli within their range of motion, but salticids have to turn to bring targets into this frontal zone in the first place. We describe how the front-facing pair of secondary eyes (anterior lateral, AL) mediates this through a series of whole-body 'tracking saccades' in response to computer-generated stimuli. We investigated the 'response area' of the AL eyes and show a clear correspondence between the physical margins of the retina and stimulus position at the onset of the first saccade. Saccade frequency is maximal at the margin of AL and AM fields of view. Furthermore, spiders markedly increase the velocity with which higher magnitude tracking saccades are carried out. This has the effect that the time during which vision is impaired due to motion blur is kept at an almost constant low level, even during saccades of large magnitude.     

Active sensing in a freely walking spider: look where to go

The Central American hunting spider Cupiennius salei, like most other spiders, has eight eyes, one pair of principal eyes and three pairs of secondary eyes. The principal eyes and one pair of the secondary eyes have almost completely overlapping visual fields, and presumably differ in function. The retinae of the principal eyes can be moved independently by two pairs of eye muscles each, whereas the secondary eyes do not have such eye muscles. The behavioural relevance of retinal movements of freely moving spiders was investigated by a novel dual-channel telemetric registration of the eye muscle activities. Walking spiders shifted the ipsilateral retina with respect to the walking direction before, during and after a turning movement. The change in the direction of vision in the ipsilateral anterior median eye was highly correlated with the walking direction, regardless of the actual light conditions. The contralateral retina remained in its resting position. This indicates that Cupiennius salei shifts it visual field in the walking direction not only during but sometimes previous to an intended turn, and therefore “peers” actively into the direction it wants to turn.     

Pathways of ocular entrainment in Marpissa marina (Araneae,Salticidae)

Depending on the animal species, photoreceptors are located in the visual organs, in non-visual organs or in both. Because of unique characteristics of vision containing several different pairs of eyes, I chose the jumping spider (salticid) Marpissa marina (Araneae: Salticidae; Goyen, 1892) for this study. Eyes in spiders are categorized in two groups of principal and secondary. Specifically, my aim was to determine which eyes are dedicated to regulation of the central circadian rhythm and to illuminate the pathway(s) of ocular entrainment in jumping spiders. To achieve this, I used an opaque elastic paste to prevent entry of light to the photoreceptors. My procedure was to measure spider activity levels over eight days as well as spiders responses to a 6 h delay shift in light/dark cycle. This would be made first with uncovered eyes (and sham covers) and then with distinct pairs of eyes covered. The results revealed that, unlike the secondary eyes, light information gathered through AMEs did not lead directly or indirectly to the parts of the circadian system that contain circadian pacemakers.     

Spiders Use Airborne Cues to Respond to Flying Insect Predators by Building Orb-Web with Fewer Silk Thread and Larger Silk Decorations

Orb-web spiders are an important group of trap-building animals that feed upon an array of insect prey and are themselves the prey of wasps and parasitoid flies. The purpose of this study was to examine whether spiders use airborne vibration cues to respond to these flying insect predators by changing their web-building behavior. While on its web waiting for prey, the orb-web spider Eriophora sagana was exposed to a vibrating tuning fork that emitted an airborne vibration signal. The signal mimicked the approach of flying insect predators and its effect on the subsequent web building was examined. No stimulus was provided during web building. A significant treatment effect was observed with respect to the total thread length (TTL) and area of the silk decoration (conspicuous white structure attached to the orb-webs of diurnal spiders) of their webs. While control spiders increased the TTL in their second web, the stimulus group spiders did not, providing the first evidence that orb-web spiders use airborne vibration cues to assess the predation risk and change their foraging activity. It also indicates that spiders remember an encounter with a predator on their webs and use this information later to adjust their web building. My findings imply that spiders devote less effort to foraging (i.e. web building) in response to the presence of their predators, which is considered to reduce their foraging efficiency. In contrast, the stimulus group spiders increased the area of their silk decoration significantly more in their second webs than did the control spiders. This is considered an experimental support for the hypothesis that silk decorations have an anti-predator function.     

The retinae of Ewyattus bleekeri, an aberrant salticid spider from Queensland

The retinal ultrastructure of an aberrant salticid spider, Euryattus bleekeri (Doleschall, 1859) is described, and discussed in the context of a model of the evolution of the Salticidae previously proposed by Jackson & Blest (1982a). The evolutionary model suggested that the Salticidae are derived from web-building ancestors that acquired the strategy of invading the webs of other species and families of spiders; it predicts that the evolution of the principal eyes preceded that of the accessory eyes, and that traces of this sequence of events should be observable in contemporary forms. Euryattus exhibits an unusual pattern of web-dependency (Jackson, 1985). The principal eyes conform to those of 'advanced' Salticidae, but the anterior lateral eyes exhibit two features associated, so far, with the primitive Spartaeinae: transverse sections of the rhabdoms present rectangular (rather than circular) profiles, and the non-pigmented glial cytoplasm is depleted of microtubules. These findings marginally support a case for Euryattus having primitive affinities, but their import is ambiguous, and the evidence cannot be regarded as conclusive. Possible affinities between the Gnaphosidae and Salticidae based upon common tactics of web-invasion are qualified by a comment on the retinae of the two families.     

The fine structure of the visual system of Lycosa (Araneae: Lycosidae)

Summary Wolf spiders have four pairs of eyes distributed in three rows. The first row which lie in the frontal region of the caparace, just above the chelicera, contains four eyes: a medial pair known as the anterior medial eyes (AM eyes or principal eyes) and two smaller eyes known as the anterior lateral eyes (AL eyes). The second row which is located also in the frontal region of the prosoma consists of two big eyes. These are the posterior median eyes (PM eyes). The third row contains the posterior lateral eyes (PL eyes) which lie in the flanks of the prosomal caparace. The AL, PM and PL eyes are the so-called secondary eyes.The electron microscope shows that the AM eye photoreceptor cells have the rhabdomere in their distal segment, just behind the vitreous body. The rhabdomere consists of closely packed microvilli about 0.5 long exhibiting a uniform diameter of 500 Å. Each rhabdom consists of two rhabdomeres. The distal segment of the photoreceptor has a prismatic shape with four or five faces depending of their location within the retina.The distribution of the rhabdoms follows two different patterns or organization. In the peripheral portion of the retina they lie oriented either parallel or perpendicular to the retinal radii. In this zone most cells have four sides while in the central region five sided cells are predominant. These cells bear microvilli in three of their five faces and the rhabdoms show no preferential mode of orientation. Each retina contains approximately 450 photoreceptors. In the secondary eyes the rhabdoms lie far from the vitreous body behind the level of the cell nuclei. A light reflecting layer or tapetum is present in the three pairs of secondary eyes. The microvilli forming the rhabdomeres of the AL eyes are 0.5 long and 500 Å wide, while the microvilli of the rhabdomeres in the PM and PL eyes are longer and thicker (1.5 long and 550–660 Å wide). In these eyes the rhabdomeres are surrounded by abundant extracellular material. Like in the principal eyes each rhabdom consists of two rhabdomeres.In the AL eyes the photoreceptor cells send out collateral branches which end, without any specialization, in contact with other photoreceptors. Clear fibers running parallely to the tapetum have been found in the secondary eyes. These fibers show specialized regions corresponding to the zones of contact with the photoreceptor cells. These areas are characterized by an increased density of the membranes and groups of vesicles (the vesicles lie within the fibers).The optic nerves consist of photoreceptor axons, glial cells and a fibrous perineural sheath. The AM and AL eyes are connected to the CNS by a single compact optic nerve while in the PM and PL eyes the optic nerve consists of several individual bundles. The total number of optic fibers entering into the brain is about 12.000.A layer of glial cytoplasm covers each photoreceptor axon and the mesaxons appear as double lines which bifurcate frequently.Research sponsored by the Air Force Office of Scientific Research, Office of Aerospace Research, United States Air Force, under AFOSR Grant Nr. 618-64.     

Maternal defensive behaviors of <Emphasis Type="Italic">Uloborus</Emphasis> sp. (Araneae,Uloboridae): behavioral repertoire and influence of clutch size and female size on female aggressiveness

Maternal care in spiders often involves behaviors associated with the protection of eggs and spiderlings against parasitoids and predators (including conspecifics). The females of several species have been documented to move their egg sacs away from natural enemies or to invest in active defense behaviors against web invaders, such as parasitoid wasps or araneophagic spider species, to protect their brood. In this study, we present observations of protective behavior by Uloborus sp. females carrying egg sacs. We also investigated whether brood size and female size influence female aggressive behaviors and response time against an artificial source of disturbance. Females carrying egg sacs almost immediately perceived and reacted aggressively against the artificial stimulus, whereas females without egg sacs moved away or ran to the web margins, avoiding the source of disturbance. The aggressive response was independent of clutch size and female body size, indicating that all females will risk interacting with potential agents of egg mortality. This systematic response by all females with egg sacs may be important for reducing the incidence of attack by the egg predator wasp Bathyzonus sp. (Ichneumonidae).     

Visual fields and eye morphology support color vision in a color-changing crab-spider

Vision plays a major role in many spiders, being involved in prey hunting, orientation or substrate choice, among others. In Misumena vatia, which experiences morphological color changes, vision has been reported to be involved in substrate color matching. Electrophysiological evidence reveals that at least two types of photoreceptors are present in this species, but these data are not backed up by morphological evidence. This work analyzes the functional structure of the eyes of this spider and relates it to its color-changing abilities. A broad superposition of the visual field of the different eyes was observed, even between binocular regions of principal and secondary eyes. The frontal space is simultaneously analyzed by four eyes. This superposition supports the integration of the visual information provided by the different eye types. The mobile retina of the principal eyes of this spider is organized in three layers of three different types of rhabdoms. The third and deepest layer is composed by just one large rhabdom surrounded by dark screening pigments that limit the light entry. The three pairs of secondary eyes have all a single layer of rhabdoms. Our findings provide strong support for an involvement of the visual system in color matching in this spider.     

The synganglion of the jumping spider Marpissa muscosa (Arachnida: Salticidae): Insights from histology,immunohistochemistry and microCT analysis

Jumping spiders are known for their extraordinary cognitive abilities. The underlying nervous system structures, however, are largely unknown. Here, we explore and describe the anatomy of the brain in the jumping spider Marpissa muscosa (Clerck, 1757) by means of paraffin histology, X-ray microCT analysis and immunohistochemistry as well as three-dimensional reconstruction. In the prosoma, the CNS is a clearly demarcated mass that surrounds the esophagus. The anteriormost neuromere, the protocerebrum, comprises nine bilaterally paired neuropils, including the mushroom bodies and one unpaired midline neuropil, the arcuate body. Further ventrally, the synganglion comprises the cheliceral (deutocerebrum) and pedipalpal neuropils (tritocerebrum). Synapsin-immunoreactivity in all neuropils is generally strong, while allatostatin-immunoreactivity is mostly present in association with the arcuate body and the stomodeal bridge. The most prominent neuropils in the spider brain, the mushroom bodies and the arcuate body, were suggested to be higher integrating centers of the arthropod brain. The mushroom body in M. muscosa is connected to first and second order visual neuropils of the lateral eyes, and the arcuate body to the second order neuropils of the anterior median eyes (primary eyes) through a visual tract. The connection of both, visual neuropils and eyes and arcuate body, as well as their large size corroborates the hypothesis that these neuropils play an important role in cognition and locomotion control of jumping spiders. In addition, we show that the architecture of the brain of M. muscosa and some previously investigated salticids differs significantly from that of the wandering spider Cupiennius salei, especially with regard to structure and arrangement of visual neuropils and mushroom body. Thus, we need to explore the anatomical conformities and specificities of the brains of different spider taxa in order to understand evolutionary transformations of the arthropod brain.     

Spider movement, UV reflectance and size, but not spider crypsis, affect the response of honeybees to Australian crab spiders

According to the crypsis hypothesis, the ability of female crab spiders to change body colour and match the colour of flowers has been selected because flower visitors are less likely to detect spiders that match the colour of the flowers used as hunting platform. However, recent findings suggest that spider crypsis plays a minor role in predator detection and some studies even showed that pollinators can become attracted to flowers harbouring Australian crab spider when the UV contrast between spider and flower increases. Here we studied the response of Apis mellifera honeybees to the presence of white or yellow Thomisus spectabilis Australian crab spiders sitting on Bidens alba inflorescences and also the response of honeybees to crab spiders that we made easily detectable painting blue their forelimbs or abdomen. To account for the visual systems of crab spider's prey, we measured the reflectance properties of the spiders and inflorescences used for the experiments. We found that honeybees did not respond to the degree of matching between spiders and inflorescences (either chromatic or achromatic contrast): they responded similarly to white and yellow spiders, to control and painted spiders. However spider UV reflection, spider size and spider movement determined honeybee behaviour: the probability that honeybees landed on spider-harbouring inflorescences was greatest when the spiders were large and had high UV reflectance or when spiders were small and reflected little UV, and honeybees were more likely to reject inflorescences if spiders moved as the bee approached the inflorescence. Our study suggests that only the large, but not the small Australian crab spiders deceive their preys by reflecting UV light, and highlights the importance of other cues that elicited an anti-predator response in honeybees.     

Fine structure of the anterior median eyes of the funnel-web spider Agelena labyrinthica (Araneae: Agelenidae)

Only few electron microscopic studies exist on the structure of the main eyes (anterior median eyes, AME) of web spiders. The present paper provides details on the anatomy of the AME in the funnel-web spider Agelena labyrinthica. The retina consists of two separate regions with differently arranged photoreceptor cells. Its central part has sensory cells with rhabdomeres on 2, 3, or 4 sides, whereas those of the ventral retina have only two rhabdomeres on opposite sides. In addition, the rhabdomeres of the ventral retina are arranged in a specific way: Whereas in the most ventral part they form long tangential rows, those towards the center are detached and are arranged radially. All sensory cells are wrapped by unpigmented pigment cell processes. In agelenid spiders the axons of the sensory cells exit from the middle of the cell body; their fine structure and course through the eye cup is described in detail. In the central part of the retina efferent nerve fibres were found forming synapses along the distal region of the receptor cells. A muscle is attached laterally to each eye cup that allows mainly rotational movements of the eyes. The optical performance (image resolution) of these main eyes with relatively few visual cells is discussed.     

Plant architectural traits influence residence time of a specialist jumping spider

The patch residence time of spiders has long been attributed to prey availability. We provide empirical evidence that plant architecture determines the residence time of a bromeliad-living spider. The residence time of spiders was longer on rosette-shaped plants. Males left their host plant faster than females, likely due to their mate-searching activity. We demonstrate that plant architectural traits mediate the patch-leaving tendency of specialist spiders.     

Dual Sensitivities of Cells in Wolf Spider Eyes at Ultraviolet and Visible Wavelengths of Light

Intracellular recordings have been made from visual cells in principal and secondary eyes of in vitro wolf spider preparations. The responses of all cells to all wavelengths of light were graded depolarizations; no hyperpolarizations or nerve discharges were seen. Cells in a secondary eye, the anterior lateral eye, had a maximum sensitivity in the visible at 510 nm and a secondary maximum, or shoulder, of sensitivity in the near ultraviolet at 380 nm. Cells in principal eyes, the anterior median eyes, all responded maximally both in the visible at 510 nm and in the ultraviolet at 360–370 nm or less. However, there was no typical ratio of ultraviolet to visible sensitivities; the differences in log sensitivities (log UV/VIS) varied from 3.3 to -0.5. Each principal eye had a population of cells with different ratios. These populations varied with the time of the year, possibly due to changes in light upon the animals. Chromatic adaptations of cells in anterior median (but not anterior lateral) eyes resulted in small, selective changes in spectral sensitivities, and there was some facilitation of responses from cells repeatedly stimulated. It is concluded that cells of secondary eyes contain only a visual pigment absorbing maximally in the visible, while cells of principal eyes probably contain variable amounts of both this pigment and one absorbing in the ultraviolet as well.     

Visually mediated motor planning in the escape response of Drosophila

A key feature of reactive behaviors is the ability to spatially localize a salient stimulus and act accordingly. Such sensory-motor transformations must be particularly fast and well tuned in escape behaviors, in which both the speed and accuracy of the evasive response determine whether an animal successfully avoids predation [1]. We studied the escape behavior of the fruit fly, Drosophila, and found that flies can use visual information to plan a jump directly away from a looming threat. This is surprising, given the architecture of the pathway thought to mediate escape [2, 3]. Using high-speed videography, we found that approximately 200 ms before takeoff, flies begin a series of postural adjustments that determine the direction of their escape. These movements position their center of mass so that leg extension will push them away from the expanding visual stimulus. These preflight movements are not the result of a simple feed-forward motor program because their magnitude and direction depend on the flies' initial postural state. Furthermore, flies plan a takeoff direction even in instances when they choose not to jump. This sophisticated motor program is evidence for a form of rapid, visually mediated motor planning in a genetically accessible model organism.     

Risky Courtship: Background Contrast,Ornamentation, and Display Behavior of Wolf Spiders Affect Visual Detection by Toad Predators

Males that search widely for females and perform conspicuous courtship displays run a high risk of being detected by their predators. Therefore, gains in reproductive success might be offset by increased mortality due to predation. Male brush‐legged wolf spiders (Schizocosa ocreata) with larger decorative traits (foreleg tufts) are preferred by females as mates, but are more readily detected by predators. However, predation risk may also be influenced by the interaction between components of signals and the environment in which signaling occurs. Courting male spiders were readily accepted as prey by a sympatric predator, the American toad (Anaxyrus americanus). We used video playback to tease apart the interactive effect between visual signals and the signaling environment on the ability of toads to detect courting spiders as a function of distance, background contrast, the presence or absence of male foreleg tufts, and behavioral activity. The response of toads to video sequences of male spiders was similar to their response to live male spiders. Toad response varied over distance toward spiders displayed against high contrast (sunny) vs. low contrast (shaded) backgrounds. Beyond 30 cm, more toads detected courting male spiders against light, ‘sunny’ backgrounds and detected them faster when compared to the same spider stimulus against darker, ‘shady’ backgrounds. In choice tests, toads oriented more often toward courting males with leg tufts than those without. Toad responses also varied with male spider behavior in that only videos of moving males were attacked. Latency to orient and detection by toads was significantly greater for walking males than courting males, and this effect was most evident at distances between 30 cm and 50 cm. Results supported that courting wolf spiders are at significant risk of predation by visually acute predators. Distance, background contrast, and the presence of foreleg decorations influence detection probability. Thus, the same complex visual signals that make males conspicuous and are preferred by females can make males more vulnerable as prey to toads.     

Antipredator benefits of group living in colonial web-building spiders: the ‘early warning’ effect

The Mexican colonial web-building spider Metepeira incrassata is frequently attacked by predatory wasps from a number of families. Previous studies have shown that wasps often attack more than one spider during a ‘run’ on a colony, but capture success declines as colony size increases, and that spiders in the central core of the colony have lower risk (Rayor & Uetz 1990, Behavioral Ecology and Sociobiology, 27, 77-85; Uetz & Hieber 1994, Behavioral Ecology, 5, 326-333). We used data from direct observation of attacks and field experiments to test the hypothesis that colonial web-building spiders benefit from ‘early warning’ of predator approach through vibrations in the colony web. Analysis of 135 naturally occurring wasp attack ‘runs’ (attacks on 454 spiders) showed that the per-attack run and per-spider capture success of wasps decreased significantly with increased spider colony size. Spider defensive and evasive behaviours observed in a subset of these attacks varied with the attack sequence. Evasive responses by spiders were more frequent later in the attack, suggesting advance warning of predator approach. Experiments using a predator-simulating vibration source demonstrated that mean reaction distance of spiders increased with increasing colony size. Adult female spiders in core positions reacted at greater distances than those on the periphery, but immature spiders, whose capture risk is lower, showed no difference. Behaviour of spiders during simulated attacks was similar to observed encounters with wasps: evasive responses were more frequent and response latency was shorter in spiders attacked later in the sequence, and in many cases, spiders took evasive action prior to any contact with the stimulus. Additional experiments testing isolated cues (web contact, airborne vibration, web-borne vibration) suggest spiders respond to web-borne vibrations generated by predators and evasive behaviours of other spiders. Together, these results support the ‘early warning’ hypothesis of antipredator benefits for colonial web-building spiders.     

Consequences of sexual size dimorphism on energetics and locomotor performance of Grammostola rosea (Araneae; Teraphosidae)

Most male spiders are smaller than females; during sexual maturity, males change their behaviour, abandoning their web or nest to seek out receptive females actively, whereas females stalk prey near their web or nest and tend not to move away from it. Considering this behavioural difference to be associated with increased locomotor activity at maturity, it may be hypothesized that males will have traits that increase locomotor performance. The present study examines the kinetics and energetics of the movements of the mygalomorph spider Grammostola rosea Walckenaer, a large spider with sexual size dimorphism. It is found that males have a higher maximum aerobic speed, average speed, distance travelled and critical angle of climbing than females, indicating better performance. Males also have lower costs of transport than females. These results support the hypothesis that sexual dimorphism in wandering spiders with active males, which are characterized by smaller body size and longer legs than the larger and more static females, is associated with low transport cost, high velocity and better locomotor performance.     

A Mechanical Model for the Adhesion of Spiders to Nominally Flat Surfaces

In dry attachment systems of spiders and geckos, van der Waals forces mediate attraction between substrate and animaltarsus. In particular, the scopula of Evarcha arcuata spiders allows for reversible attachment and easy detachment to a broadrange of surfaces. Hence, reproducing the scopula’s roughness compatibility while maintaining anti-bunching features and dirtparticle repellence behavior is a central task for a biomimetic transfer to an engineered model. In the present work we model thescopula of E. arcuata from a mechano-elastic point of view analyzing the influence of its hierarchical structure on the attachmentbehavior. By considering biological data of the gecko and spider, and the simulation results, the adhesive capabilities of thetwo animals are compared and important confirmations and new directives in order to reproduce the overall structure are found.Moreover, a possible suggestion of how the spider detaches in an easy and fast manner is proposed and supported by the results.     

Crab spiders deter insect visitations to slickspot peppergrass flowers

Insects visiting the flowers of slickspot peppergrass, Lepidium papilliferum (Brassicaceae), risk predation by crab spiders, Misumena vatia (Thomisidae). In a field study conducted at two sites in southwestern Idaho, 7.5±2.7% of L. papilliferum plants (range 0–30%, N=16 surveys of up to 40 randomly selected plants) harbored a crab spider. However, through 205 minutes of observations at plants with a spider, only 15 predation attempts were observed, with only 3 of those being successful. Despite the relatively low incidence of predation by crab spiders, an experiment revealed that the number of insects visiting L. papilliferum flowers was significantly lower at plants that harbored a crab spider than at plants free of spiders. In another experiment, floral visits increased significantly following the removal of crab spiders from individual plants. The deterrent effect of spiders was not due to a disproportionate avoidance response by certain types of insects; all insect families included in our analysis showed decreases in visitations to flowers when spiders were present, although none of these differences were statistically significant at the individual level. We found no significant change in the duration of visits to plants harboring a spider, implying either that the visitors were oblivious to the predator's presence, or that they were aware of the predator but kept their distance. Our study is one of a growing number to find a decrease in floral visits in response to predators, suggesting that the phenomenon is more widespread than was previously recognized.     

On the Relationships between Ground-dwelling Spider (Araneae) Assemblages and Dead Wood in a Northern Sugar Maple Forest

Downed woody material (fallen logs) offers ground-dwelling spiders (Araneae) ideal sites for nesting and foraging, but little is known about what characteristics of dead wood influence spider assemblages. In a maple forest of Forillon National Park, in eastern Québec (Canada), spider assemblages on, adjacent to, and away from fallen logs were compared. We also tested how log type (coniferous vs. deciduous) and decomposition stage influenced spider assemblages. Sampling was done for an intensive four-week period using both litter samples and pitfall traps. A total of 5613 spiders representing 83 species from 16 families was collected. Spiders were affected by the presence of logs, as both species diversity and total number of individuals collected were significantly higher on the log surface compared to the forest floor. Ordination analysis revealed a distinct compositional difference between the spider fauna found on the wood surface compared to the forest floor. Wood type and decomposition stage had few significant effects on spider assemblages, except that less decayed logs supported higher spider diversity than logs in advanced stages of decay. Dead wood is clearly important for generalist predators such as spiders, further supporting the conservation importance of fallen logs in northern forest ecosystems.