Salticidae Research Articles

Spider eyes inspire compact camera

Jumping spiders are brilliant hunters, accurately leaping relatively large distances to surprise their prey. They can plan these surprise pounces just right thanks to their fantastic depth perception. Each of their two principal eyes has a double-layered retina. Spider behaviorists believe the creatures use their poppy-seed-sized brains to compare the relative sharpness of the two images from the two retinal layers and use that information to estimate distances. “We’re still not 100% sure how spiders actually achieve this because we don’t read spider minds,” says Zhujun Shi, a grad student in physics at Harvard University. Still, she and collaborators Qi Guo and Federico Capasso were inspired by the critters and decided to mimic their retinas to make a simple depth-sensing camera that could lead to simple, low-power sensors for cell phones and robots (Proc. Natl. Acad. Sci. U.S.A. 2019, DOI: 10.1073/pnas.1912154116). Existing systems require an infrared light source or moving

Compact single-shot metalens depth sensors inspired by eyes of jumping spiders

Jumping spiders (Salticidae) rely on accurate depth perception for predation and navigation. They accomplish depth perception, despite their tiny brains, by using specialized optics. Each principal eye includes a multitiered retina that simultaneously receives multiple images with different amounts of defocus, and from these images, distance is decoded with relatively little computation. We introduce a compact depth sensor that is inspired by the jumping spider. It combines metalens optics, which modifies the phase of incident light at a subwavelength scale, with efficient computations to measure depth from image defocus. Instead of using a multitiered retina to transduce multiple simultaneous images, the sensor uses a metalens to split the light that passes through an aperture and concurrently form 2 differently defocused images at distinct regions of a single planar photosensor. We demonstrate a system that deploys a 3-mm-diameter metalens to measure depth over a 10-cm distance range, using fewer than 700 floating point operations per output pixel. Compared with previous passive depth sensors, our metalens depth sensor is compact, single-shot, and requires a small amount of computation. This integration of nanophotonics and efficient computation brings artificial depth sensing closer to being feasible on millimeter-scale, microwatts platforms such as microrobots and microsensor networks.

Euophrys petrensis C. L. Koch, 1837, is a genuine member of the genus Talavera (Araneae: Salticidae)

Euophrys petrensis C. L. Koch, 1837, is a genuine member of the genus Talavera (Araneae: Salticidae)

The behavioral repertoire of Drosophila melanogaster in the presence of two predator species that differ in hunting mode.

The fruit fly, Drosophila melanogaster, has proven to be an excellent model organism for genetic, genomic and neurobiological studies. However, relatively little is known about the natural history of D. melanogaster. In particular, neither the natural predators faced by wild populations of D. melanogaster, nor the anti-predatory behaviors they may employ to escape and avoid their enemies have been documented. Here we observe and describe the influence of two predators that differ in their mode of hunting: zebra jumping spiders, Salticus scenicus (active hunters) and Chinese praying mantids, Tenodera sinensis (ambush predators) on the behavioral repertoire of Drosophila melanogaster. We documented three particularly interesting behaviors: abdominal lifting, stopping, and retreat—which were performed at higher frequency by D. melanogaster in the presence of predators. While mantids had only a modest influence on the locomotory activity of D. melanogaster, we observed a significant increase in the overall activity of D. melanogaster in the presence of jumping spiders. Finally, we observed considerable among-individual behavioral variation in response to both predators.

The role of male coloration and ornamentation in potential alternative mating strategies of the dimorphic jumping spider, Maevia inclemens

Polymorphism can arise across taxa due to various selection pressures and potentially lead to alternative mating or antipredator strategies. For male jumping spiders, sexual selection and predation risk are often intertwined when courting cannibalistic females and may be a driving factor in the polymorphism of the jumping spider, Maevia inclemens. The dimorphic males of M. inclemens differ dramatically in their complex courtship behavior and display traits that may function as alternative mating strategies to reduce female aggression and maximize mating success. We hypothesized that males of the “tufted” morph honestly communicate condition or body size to females with three conspicuous tufts of setae on their head and males of the “striped” morph reduce female aggression with coloration commonly found in aposematic animals (here, yellow-orange pedipalps and striped legs). We examined correlations between tuft length and symmetry and metrics of body size and condition in field-collected spiders and conducted prey color choice tests (with live color-manipulated prey) to determine if yellow-orange and striped prey are avoided. Tuft length was variable and correlated with male size (but not condition). All prey color types were attacked at equal rates, but spiders oriented to striped prey more often, suggesting that male stripes may attract female attention without increasing predation. This study provides insight into the potential functions of the different courtship and visual displays of M. inclemens males. Using jumping spiders to study polymorphism can provide new insight into how multiple morphs can evolve, as males use mating strategies not only to impress females but also avoid getting eaten by their potential mates.Significance statementUnderstanding the selection pressures that shape and maintain polymorphisms in natural populations is an active area of inquiry, yet most of what we know comes from a small handful of well-studied vertebrate taxa. The unique biology of jumping spiders and the fact that males have to avoid cannibalism during courtship, makes them well-suited to provide novel insights into the functions and maintenance of dimorphic male traits. The unusual male dimorphism of M. inclemens captured the attention of naturalists as early as the 1800s, yet we still do not understand why the two male morphs differ so dramatically in morphology and courtship behavior. Here, we propose and test a novel hypothesis that provides insight into the long-studied but still largely unexplained phenomenon of male dimorphism in this species.

Manipulation of Color Patterns in Jumping Spiders for Use in Behavioral Experiments.

In the field of behavioral ecology, many experiments are designed to investigate the evolutionary purposes of colorful traits in the context of sexual selection and predation. Methods are various but mostly consist of modifying the color patterns of individuals with diverse colorants. Such techniques have been used across many vertebrate taxa, particularly in birds, but have remained underdeveloped for invertebrates because of the difficulty of effectively manipulating color in small organisms. Instead, to manipulate the appearance of invertebrates, scientists have usually modified the lighting environment to filter out certain wavelengths. However, such a method affects not only the phenotypic trait of interest but the entire appearance of the individual and its surrounding. Here, scaling down the techniques previously used on colorful birds, we present ways of manipulating the colors of small arthropods, using equally emblematic but understudied species: the colorful jumping spiders.

Growing tiny eyes: How juvenile jumping spiders retain high visual performance in the face of size limitations and developmental constraints

Adult jumping spiders are known for their extraordinary eyesight and complex, visually guided behaviors, including elaborate communicatory displays, navigational abilities, and prey-specific predatory strategies. Juvenile spiders also exhibit many of these behaviors, yet their visual systems are many times smaller. How do juveniles retain high visually guided performance despite severe size constraints on their visual systems? We investigated developmental changes in eye morphology and visual function in the jumping spider Phidippus audax using morphology, histology, ophthalmoscopy, and optical measurements. We find that juvenile spiders have proportionally larger lenses in relation to their body size than adults. This should alleviate some of the costs of small body size on visual function. However, photoreceptor number in the anterior lateral eyes (ALE) remains constant from early development onward, consistent with a developmental constraint on photoreceptor differentiation. To accommodate these photoreceptors within the diminutive volume of the spiderling cephalothorax, ALE rhabdoms in early life stages are more tightly packed and significantly smaller in diameter and length, properties that expand across development. Lens focal lengths increase as eyes and retinas grow, resulting in a remarkable maintenance of ALE spatial acuity and field-of-view across life stages. However, this maintenance of acuity comes at a sensitivity cost given the small rhabdomal volumes required by space constraints early in life. Taken together, our results indicate that young jumping spiders have eyes already equipped for high acuity vision, but these young spiders may struggle to perform visually demanding behaviors in low-light environments, a notion that warrants further testing.

Photoreceptor projection from a four-tiered retina to four distinct regions of the first optic ganglion in a jumping spider.

Jumping spiders have four pairs of eyes (ocelli) of which only the principal eyes (PEs) are used to detect features of objects. Photoreceptors in the retina of the PEs form four layers (PL1-4) and terminate in the first optic ganglion (FOG). Here, we focus on Hasarius adansoni because it has unique depth vision besides color vision and its FOG appears to contribute to the initial processing of these visual modalities. We first investigated the neuroanatomical organization of the FOG. The three-dimensional structure of the FOG revealed by synapsin immunostaining is horseshoe-shaped and consists of four terminal zones (TZ1-4). Then, we traced single photoreceptors through serial sections and found that green-sensitive receptors of PL1 and 2 terminate in TZ1 and 2, respectively, by keeping retinotopic organization. In contrast to TZ1 and 2, TZ3 receives terminals of ultraviolet-sensitive receptors from lateral regions of both PL3 and 4, while photoreceptors of the medial region of PL3 and 4 terminate in TZ4. We further studied details of photoreceptor terminals and the branching pattern of interneurons in the FOG in Golgi stained preparations. Photoreceptors have long lateral processes in each terminal zone. Some photoreceptors terminating in TZ3 have branches innervating TZ1, indicating that TZ1 receives different spectral information. A type of interneuron connects TZ1 and 2, while others have branches within a single terminal zone or in the entire FOG. These results suggest that TZ1 and 2 contribute to color, shape, and depth vision, while TZ3 and 4 have specific roles for UV vision.

Dim-light vision in jumping spiders (Araneae, Salticidae): identification of prey and rivals.

Jumping spiders (family Salticidae) are known for their intricate vision-based behavior during encounters with prey and conspecific individuals. This is achieved using eyes specialized for discerning fine detail, but there has been minimal research on the capacity that salticids might have for visual performance under low ambient light levels. Here, we investigated the capacity of two salticid species, Cyrba algerina from Portugal and Cyrbaocellata from Kenya, to perform two specific visual tasks under low ambient light levels. We used lures made from spiders and midges in prey-identification experiments and mirror images (virtual conspecifics) in rival-identification experiments. These experiments were implemented under a range of ambient light levels (234, 1.35, 0.54, 0.24 cd m-2). In most instances, Calgerina and Cocellata were proficient at performing both of these visual tasks when ambient light was 234 and 1.35 cd m-2, and a minority performed these tasks at 0.54 cd m-2, but none succeeded when the light level was 0.24 cd m-2Cyrbaalgerina and C. ocellata showed vision-based discrimination under low ambient light levels previously associated with nocturnal species.

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

ABSTRACTDepending 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.

Further Additions to the Jumping Spider Fauna of South Africa (Araneae: Salticidae)

Examination of museum collections and of recently collected materials from South Africa lead to the discovery of the following eight new jumping spider species that are described here: Evarcha amanzi sp. nov. (♂), E. villosa sp. nov. (♂), Langellurillus squamiger sp. nov. (♂♀), Massagris maculosa sp. nov. (♂ ♀), Microbianor simplex sp. nov. (♂), Pseudicius procerus sp. nov. (♂ ♀), Rhene legitima sp. nov. (♂) and Thyenula splendens sp. nov. (♂ ♀). Massagris concortuplicata Wesolowska & Haddad, 2013 syn. nov. is newly synonymized with M. mirifica Peckham & Peckham, 1903, and both sexes are redescribed. The unknown males of Asemonea amatola Wesolowska & Haddad, 2013, Heliophanus gramineus Wesolowska & Haddad, 2013 and Menemerus rubicundus Lawrence, 1928, and the unknown females of H. sororius Wesolowska, 2003, Massagris natalensis Wesolowska & Haddad, 2009, Microbianor furcatus Haddad & Wesolowska, 2013, Rhene amanzi Wesolowska & Haddad, 2013 and R. pinguis Wesolowska & Haddad, 2009 are described for the first time. The females of Menemerus rubicundus and Neaetha irreperta Wesolowska & Russell-Smith, 2000, and males of Evarcha acuta Wesolowska, 2006, E. karas Wesolowska, 2011 and Habrocestum luculentum Peckham & Peckham, 1903, are redescribed. Seven species are recorded from South Africa for the first time: Belippo calcarata (Roewer, 1942), Dendryphantes acutus Wesolowska & Haddad, 2014, Evarcha acuta, E. karas, M. rubicundus, N. irreperta and Pseudicius matabelensis Wesolowska, 2011. Additionally, new provincial records for species previously recorded from elsewhere in South Africa are provided for the Eastern Cape and KwaZulu-Natal (five spp. each), Free State (three spp.), Northern Cape (two spp.), and Limpopo and Mpumalanga provinces (one sp. each).

Mating and egg-laying behavior of Hasarius adansoni (Araneae: Salticidae) and the influence of sexual selection

Jumping spiders perform multi-modal displays during courtship and this has been used to study sexual selection and mate choice. However, studies have focused on only a few groups of spiders. Here we describe for the first time the breeding behavior of the tropical jumping spider Hasarius adansoni (Audouin, 1826). Animals were collected in the field and reared in the laboratory until adulthood. We took male body measurements, paired couples in mating trials, and then collected subsequent clutches. We confirmed the presence of a multi-modal display with visual and vibratory signals (tremulations) by the males. Females responded with their own tremulations and occasionally a receptive posture. Otherwise, they avoid mating by attacking or running away from the male. No measured male morphological attributes were important for male mating success and future studies should focus on other morphological measurements to understand how the mate choice process functions in this species. Multiple matings were common and females laid numerous clutches while enclosed in silk cocoons. Number of young per clutch decreased over the course of laying bouts.

New jumping spiders from the alpine meadows of the Valley of Flowers, western Himalayas, India (Araneae, Salticidae).

Two new jumping spider species: Nandiciusvallisflorumsp. n., (♀) and Pelleneshimalayasp. n. (♂, ♀), are diagnosed, described and illustrated in detail. The specimens were collected from the Valley of Flowers, western Himalayas, Uttarakhand State of India.

Psychophysical investigation of vigilance decrement in jumping spiders: overstimulation or understimulation?

The inability to maintain signal detection performance with time on task, or vigilance decrement, is widely studied in people because of its profound implications on attention-demanding tasks over sustained periods of time (e.g., air-traffic control). According to the resource depletion (overload) theory, a faster decrement is expected in tasks that are cognitively demanding or overstimulating, while the underload theory predicts steeper decrements in tasks that provide too little cognitive load, or understimulation. Using Trite planiceps, a jumping spider which is an active visual hunter, we investigated vigilance decrement to repetitive visual stimuli. Spiders were tethered in front of two stimulus presentation monitors and were given a polystyrene ball to hold. Movement of this ball indicates an attempt to turn towards a visual stimulus presented to a pair of laterally facing (anterior lateral) eyes for closer investigation with high acuity forward-facing (anterior median) eyes. Vigilance decrement is easily measured, as moving visual stimuli trigger clear optokinetic responses. We manipulated task difficulty by varying the contrast of the stimulus and the degree of 'noise' displayed on the screen over which the stimulus moved, thus affecting the signal:noise ratio. Additionally, we manipulated motivation by paired testing of hungry and sated spiders. All factors affected the vigilance decrement, but the key variable affecting decrement was stimulus contrast. Spiders exhibited a steeper decrement in the harder tasks, aligning with the resource depletion theory.

Odor alters color preference in a foraging jumping spider.

In many prey taxa with aposematic coloration, prey defenses also involve signals in other modalities (odors, sounds, etc.), yet the selective forces that have driven multimodality in warning displays are not well understood. One potential hypothesis that has recently received support in the avian literature (but has yet to be examined in invertebrates) is that different signal components may interact synergistically, such that one component of a signal (odor) may trigger a predator’s aversion to another component of a signal (color). Here, we gave jumping spiders (Habronattus trimaculatus) the choice between red or black prey (artificially colored termites) in either the presence or absence of odor from the chemically defended coreid bug (Acanthocephala femorata). When the odor was present, spiders were more likely to avoid the color red compared with when the odor was absent. Interestingly, this pattern only held up when the odor was novel; subsequent exposure to the odor had no effect on color preference. Moreover, this pattern only held for the color red (a color typically used as a warning color and often paired with odor). We replicated this experiment giving spiders the choice between green or black prey, and found that the presence of the odor had no effect on the spiders’ responses to the color green. We discuss these findings in the context of predator psychology and the evolution of prey coloration.

Aggressive spiders make the wrong decision in a difficult task

Accurate and timely decisions are critical for foraging, predator avoidance, and reproductive success. However, there is often a trade-off between speed and accuracy in decision-making, where individuals that make decisions more quickly make more mistakes. An individual's personality may influence its decision-making style (i.e., whether it errs more in the speed or accuracy of a decision) and this relationship may change depending on contexts. Despite growing research on invertebrate personality, how personality correlates with decision-making style is still largely unknown and little research has assessed these relationships across tasks of varying difficulty. Here, we test the relationship between aggressiveness and decision-making style in Portia labiata, a specialized spider-eating jumping spider, in both a simple and a difficult task. We found that aggressive spiders made fewer directional changes before completing the tasks, regardless of task difficulty. However, decision accuracy was jointly determined by both aggressiveness and task difficulty. Aggressive spiders made more accurate decisions in the simple task, while docile spiders made more accurate decisions in the difficult task. We conclude that the relationship between personality and decision-making style in P. labiata is context dependent. We also discuss how the association between aggressiveness and decision-making style may serve important functions in maintaining behavioral variation in a natural population.

Energy and time optimal trajectories in exploratory jumps of the spider Phidippus regius

Jumping spiders are proficient jumpers that use jumps in a variety of behavioural contexts. We use high speed, high resolution video to measure the kinematics of a single regal jumping spider for a total of 15 different tasks based on a horizontal gap of 2–5 body lengths and vertical gap of +/−2 body lengths. For short range jumps, we show that low angled trajectories are used that minimise flight time. For longer jumps, take-off angles are steeper and closer to the optimum for minimum energy cost of transport. Comparison of jump performance against other arthropods shows that Phidippus regius is firmly in the group of animals that use dynamic muscle contraction for actuation as opposed to a stored energy catapult system. We find that the jump power requirements can be met from the estimated mass of leg muscle; hydraulic augmentation may be present but appears not to be energetically essential.

Aspects of courtship risks and mating success in the dimorphic jumping spider, Maevia inclemens (Araneae: Salticidae)

The jumping spider Maevia inclemens (Walckenaer, 1837) is unusual because there are two male types, tufted (T) and gray (G). We investigated the risks of predation associated with the different courtship strategies by testing the response of the predatory jumping spider Phidippus audax (Hentz, 1845) to T and G courtship display, to ascertain if the two morphs were equally noticeable. We then tested the courting responses of T and G in the presence of a conspecific mate and a potential predator (P. audax). For the first experiment, we used computer-animation techniques to present two different views of courting males: face-on view as a female might see a courting male; and 45°-above view as may be seen from the perspective of a predator hunting in the vegetation. Visual orientation distance to the courting male images was used as an estimate of predation risk. Results demonstrated that risk of visual detection was not equal for the males; P. audax oriented to G at significantly greater distances than to T. From the 45°-above view, the apparent size of courting G males measured approximately three times greater than that of T males, suggesting that from this point of view, T may be less conspicuous to predators. In our second experiment, T and G responded differently when courting a conspecific female if a live predator had recently been or remained in view of the male. Fewer G males courted than T males and the courtship latency was significantly longer for G than for T. The visibility of T and G males to both females and potential predators may help to understand how these different, but equally successful, courtship strategies are maintained.

Mismatch between dietary requirements for lipid by a predator and availability of lipid in prey

Growth is an important factor in predicting an organism's overall success as an adult. Understanding how abiotic and biotic factors influence body size is key to predicting how environmental changes will impact organisms and predicting optimal behaviors under varying conditions. Food items can vary widely in nutrient content and this variation can affect growth. We tested how the quantity and macronutrient content of live prey affected the growth of juvenile jumping spiders, Phiddipus audax, using 420 spiderlings raised on one of 21 diets. In addition, we measured the nutrient content of prey from the field and compared average prey nutrient content with the diet at which spiders maximized growth. Our results show that the quantity and nutrient content of prey have significant and interacting effects on the growth of an actively hunting predator. In particular, spiders grew larger in body size (tibia/patella length and posterior lateral eye width) and were heavier on diets with higher lipid content. Yet, data on the nutrient content of prey from the field shows that most potential prey have high protein and low lipid content in their bodies. This apparent mismatch between spider nutritional requirements and prey nutrient availability likely presents a challenge to spiders seeking to maximize growth in the field. Several hypotheses for how these predators overcome this challenge to reach the large body sizes observed in the field are discussed.

Laboratory-reared and field-collected predators respond differently to same experimental treatments

Laboratory studies of animal behavior can use animals with different developmental histories, including those that have spent most of their lives in the field or those raised in the laboratory. Both types of animals are assumed to respond similarly to experimental treatments. The goal of this study was to test if this assumption is true, if field-collected and lab-reared animals respond similarly to experimental treatments. In the first experiments, we test how diet (high lipid or protein) affected mating behaviors of male jumping spiders, Phidippus audax. Male spiders had opposite responses to diet based on their rearing condition in both scramble competition and male-male interaction trials. Field-collected spiders fed with high-protein diets and lab-reared spiders fed with high-lipid diets found mates quicker and were more aggressive than their counter parts fed with different diets. Field-collected spiders were also more active in open arenas and courted females more actively than lab-reared spiders. In a second experiment, we tested spiders for preference of flower color, and found that both lab-reared and field-collected spiders selected flowers with color over white flowers. However, field-collected spiders prefer red flowers with UV fluorescence, while lab-reared spiders seem to prefer red without UV. These results suggest that lab-reared and field-collected animals can respond differently to the same experimental treatments. Further work is needed to test if this happens in other animals, and which types of individuals (lab-reared or field collect) best reflect the responses of animals in nature. Laboratory studies are commonly used to study animal behavior. Animals used in these studies can be either raised in the laboratory or collected from the field just prior to the study. While lab-reared and field-collected animals can differ sometimes in their behavior (e.g., more or less active in response to a treatment), they are both assumed to respond in qualitatively the same manner. However, this does not appear to be the case in our study of a common species of jumping spider, Phidippus audax. Lab-reared and field-collected animals responded in opposite directions to identical treatment conditions. These results suggest that the developmental histories of animals can fundamentally affect how they respond to experimental treatments in the laboratory and, hence, the conclusions drawn from such studies.