J. Andrew Roberts

Multisensory cues and multimodal communication in spiders: Insights from video/audio playback studies

Spiders perceive the world using multiple sensory modes, including vibration, vision, and chemical senses, for prey detection and communication. These sensory modes are used in many communication contexts, either individually or in multimodal signaling. Selection for effective signaler-receiver communication and species discrimination is especially strong for these predatory and potentially cannibalistic arthropods, resulting in the evolution of considerable diversity in signaling behaviors. In this paper, we review sensory mechanisms involved in spider signaling and present an overview of recent work done on wolf spiders (Lycosidae) that use multimodal communication (simultaneous visual and vibratory signals) in sexual signals during courtship. The relative importance of visual and vibratory signaling modes, and the use of multiple modes varies among closely related species in the genus Schizocosa, providing a model system for investigating multisensory guidance of complex behavior. Here we examine previous and current research on responses of female spiders to components of male courtship behavior, using several experimental techniques including cue isolation (single sensory modes), video/audio digitization and playback, and cue-conflict (mixed conspecific/heterospecific components) to tease apart elements of multimodal signaling.

Information content of female chemical signals in the wolf spider, Schizocosa ocreata : male discrimination of reproductive state and receptivity

Fine-scale information content of chemical signals has been widely studied in several vertebrate taxa and in social and economically important invertebrate taxa but remains poorly understood for many invertebrate predators such as spiders. Chemical signals (e.g. pheromones) associated with spider silk may convey information about species identity, sex, age and/or reproductive status of a female to male receivers. In the wolf spider Schizocosa ocreata (Hentz), females are cryptic within the leaf-litter habitat, are potentially aggressive and/or cannibalistic depending on reproductive status and age, and do not appear to communicate their status to males using seismic or visual signals. Hence, males are expected to exploit female chemical signals to discriminate among potential mates. We used behavioural assays to determine whether male S. ocreata can discriminate potentially receptive mates using cues associated with female silk. Males were presented with silk from females that varied in reproductive status and/or potential receptivity. Males showed significantly more and longer bouts of chemosensory and courtship behaviours, with significantly reduced latency, on the silk of adult, unmated female spiders than on any other stimulus treatment, including the silk of subadult and mated females. Additionally, male S. ocreata responded less to the silk cues of females that were within 1 week prior to maturity and the silk of females that had recently moulted (females up to 1 week old). This is significant, as females show increased aggression to males during their first week of adulthood and after mating. Thus, males clearly possess the ability to assess reproductive status as well as age-related potential receptivity of conspecific females based on cues associated with silk.

Multimodal communication and mate choice in wolf spiders: female response to multimodal versus unimodal signals

Male wolf spiders (Lycosidae) in the genus Schizocosa vary in use of seismic and visual components of courtship display, ranging from unimodal (seismic only) to multimodal (seismic and visual). Studies show that variation in individual modes influences female receptivity, but responses to isolated signals may not be equivalent. To examine redundancy and interaction between modes, we compared female responses to isolated and combined courtship signals from males of two sympatric sibling species that differ in use of visual and seismic modes, S. ocreata and S. rovneri. Females of both species detected multimodal stimuli faster than visual or seismic cues alone, but they differed in responses to cues once they oriented. Female S. ocreata approached males performing isolated visual and seismic cues with equal frequency, but approached males performing multimodal cues more often. A greater proportion of female S. ocreata responded more receptively to multimodal cues than to seismic or visual cues alone, and showed higher rates of receptivity displays with multimodal cues. In contrast, female S. rovneri showed no differences in approaches, but responded more often and with higher display rates to seismic cues alone or multimodal cues, but not visual cues. These results suggest multimodal signalling increases detection of males by females, but that use of signal modes varies between even closely related sibling species. For S. rovneri, male signals in different modes are nonredundant, with seismic cues dominant over visual cues when presented alone or in multimodal signals. In contrast, for S. ocreata, male signals in different modes are redundant (eliciting the same responses from females with similar frequency), while the greatly increased responsiveness to multimodal signals indicates multiplicative enhancement.

Male signaling behavior and sexual selection in a wolf spider (Araneae: Lycosidae): a test for dual functions

Male signaling behaviors are often studied in a single context but may serve multiple functions (e.g., in male–male competition and female mate choice). We examined the issue of dual function male signals in a wolf spider species Schizocosa ocreata (Hentz) that displays the same species-specific signaling behaviors in both male–male and male–female contexts. These signaling behaviors have been described as either aggression or courtship according to the context observed. We tested the possibility of dual functions by comparing the relationship between behaviors and outcome of male–male contests (winner/loser) and male–female mating encounters (mating success). Frequency, rate, and mean duration of signaling behaviors did not vary with outcome of male–male contests, which appears instead to be based upon relative size and body mass. Winners of contests had significantly greater body mass than losers, and greater mass relative to opponents was significantly associated with probability of winning. Overall, signaling rates were much higher in male–female interactions than in male–male contests and were higher for males that successfully mated than for those that did not mate. Mean duration of some male displays was also greater for males that successfully mated. However, male size was not associated with probability of mating. Taken together, results suggest an intersexual selection context for the current function of male signals in these wolf spiders and that increased display vigor is associated with male mating success.

Chemical signaling in a wolf spider: a test of ethospecies discrimination.

Chemical signals from female wolf spiders that elicit exploratory behavior and courtship in males are often assumed to be species-specific, but males of some species court in response to silk cues deposited by closely related heterospecific females. Such is the case with the wolf spiders Schizocosa ocreata and S. rovneri, ethospecies reproductively isolated on the basis of differences in behavioral mechanisms during courtship. We explored whether male S. ocreata and S. rovneri reciprocally discriminate species-specific chemical or mechanical cues associated with female silk by using male behavioral response as an assay. Males were exposed to stimulus treatment categories including silk, washed silk, silk extract, and appropriate controls within conspecific or heterospecific female stimulus categories. Male S. ocreata and S. rovneri did not discriminate between conspecific or heterospecific female stimuli, and courtship intensity was greatest on untreated silk. There were no differences in latency to begin courtship or in rates of courtship behaviors attributed to species origin of silk. However, silk treatment (washed silk, extract) had a significant effect on display and exploratory behaviors (e.g., chemoexplore) in both species. Methanol extraction of female silk successfully removed or inactivated a component necessary to elicit active courtship, but extraction did not significantly reduce exploratory behavior, suggesting that a separate compound may be responsible for releasing this behavior. Together, these experiments support the characterization of S.~ocreata and S. rovneri as ethospecies reproductively isolated only by female discrimination of species-specific male courtship, and indicate that chemical, but not mechanical cues associated with silk are critical for eliciting male courtship in both species.

Flexibility in the multi-modal courtship of a wolf spider, Schizocosa ocreata

Male Schizocosa ocreata wolf spiders court females with synchronous visual and seismic displays. We tested whether male S. ocreata modify their courtship in relation to light environment, and associated utility of the visual components. Males were generally more active and more likely to perform the major courtship element (‘jerky tapping’) when in the light. One courtship element (‘arching’) was only observed in the light while another (‘vertical leg-extend’) was only observed in the dark. Courtship in the dark retained ‘visual’ components, suggesting spiders cannot disengage these components of multi-modal display even when superfluous. Once initiated, there was no evidence that performance rate or time spent in each courtship element differed in the light and in the dark.

Kinship and food availability influence cannibalism tendency in early-instar wolf spiders (Araneae: Lycosidae)

For potentially cannibalistic animals such as spiders, the ability to recognize and avoid kin and/or preferentially cannibalize non-relatives would permit exploiting conspecifics as prey while minimizing loss of inclusive fitness. We investigated the effects of relatedness and availability of alternative food on cannibalism tendency in pairs of juvenile Hogna helluo (Walckenaer), a North American wolf spider (Araneae: Lycosidae). For second-instar spiderlings (dispersing stage), cannibalism was more likely among pairs of non-sibs than pairs of sibs and, interestingly, was also more likely when other prey were available. We found no evidence of increased cannibalism in pairings involving broods of greatest average size disparity, indicating that size differences are unlikely to explain differences in cannibalism tendency. Additionally, the relative number of deaths from cannibalism or other causes did not increase with increasing risk of starvation. For third-instar spiderlings, which had lived independently of their mother and sibs following dispersal, cannibalism rates were very high in all treatments and there were no significant effects of relatedness or food availability. Our results suggest that spiders with predominantly solitary lifestyles may bias cannibalism toward non-kin during the juvenile associative period, and that this effect is lost in the subsequent instar. Results are discussed in the context of several potential mechanisms that might result in differential cannibalism.

Species-specificity of chemical signals: Silk source affects discrimination in a wolf spider (Araneae: Lycosidae)

Female spiders deposit chemical cues that elicit male courtship behavior with silk. These cues are often assumed to be species-specific although male spiders may court in response to chemical cues of closely-related species. We used behavioral assays to test the extent of species discrimination of female chemical cues by male Schizocosa ocreata, a wolf spider (Lycosidae). Discrimination, expressed as relative courtship intensity of males, varied significantly with phylogenetic distance. Males did not discriminate between female cues of conspecifics and a sibling species, S. rovneri. Courtship response was intermediate for another species within the ocreata clade and not different from control for spiders outside the clade. These findings support the sibling species status of S. ocreata and S. rovneri, and also suggest the composition of female chemical signals is conserved across closely related wolf spider species.

Effect of visual background complexity and light level on the detection of visual signals of male Schizocosa ocreata wolf spiders by female conspecifics

For visual signaling to be effective, animal signals must be detected and discriminated by receivers, often against complex visual backgrounds with varying light levels. Accordingly, in many species, conspicuous visual displays and ornaments have evolved as a means to enhance background contrast and thereby increase the detection and discrimination of male courtship signals by females. Using video playbacks, we tested the hypothesis that visual courtship displays and leg decorations of male Schizocosa ocreata wolf spiders are more conspicuous against complex leaf-litter backgrounds. Video exemplars of courting males with manipulated leg tufts were superimposed on different backgrounds (complex leaf litter in sun or shade, featureless gray background) and presented to female spiders. Females were more likely to orient to males presented against lighter backgrounds (litter in sun, gray) than the darker ones (litter—shade). Males with larger tufts were also more likely to be detected, as latency to orient was shortest for enlarged and longest for removed tufts. Latency of females to approach was shorter against lighter backgrounds, and approach latency was longest for males without tufts. Female receptivity scores were significantly greater for males against lighter backgrounds, and males with larger tufts had higher scores. These results suggest that both complexity and light level of display backgrounds affect the detection of male visual courtship signals by females and that aspects of the male phenotype may increase chances of detection (and receptivity) against visually complex backgrounds.

Spectral reflectance and communication in the wolf spider, Schizocosa ocreata (Hentz): simultaneous crypsis and background contrast in visual signals

Animal color patterns often reflect a compromise between natural selection for crypsis or inconspicuousness to predators and sexual selection for conspicuousness to potential mates. In leaf litter-dwelling wolf spider species like Schizocosa ocreata, body coloration often closely matches the background coloration of a generally brown environment. However, body parts used in communication should exhibit high contrast against background coloration. We used spectral analysis to examine male and female S. ocreata for matching and contrasting coloration against leaf litter. Values were plotted in multivariate color space, based on reflectivity in different frequency ranges. When viewed from above, colors of both males and females overlap with values for dead brown leaf litter and soil, suggesting cryptic coloration when viewed by potential predators. However, when viewed from a lateral perspective, both males and females show color values that are polar opposites of litter backgrounds, suggesting higher contrast when viewed by other spiders. Moreover, male secondary characters used in visual signaling by S. ocreata (tibia brushes) show the highest level of background contrast. These findings suggest that S. ocreata wolf spiders have color patterns that provide both crypsis and background contrast at the same time, depending on receiver viewing perspective.