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Bruce Cutler and Sean Walker identified many of the species used in this study. Voucher specimens are on deposit at the. National Museum of Natural History in ...
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C 2004) Journal of Insect Behavior, Vol. 17, No. 4, July 2004 (°

Species-Specificity of Chemical Signals: Silk Source Affects Discrimination in a Wolf Spider (Araneae: Lycosidae) J. Andrew Roberts1,2 and George W. Uetz1 Accepted March 17, 2004; revised May 10, 2004

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. KEY WORDS: chemical communication; Schizocosa ocreata; species recognition; silk; wolf spider.

INTRODUCTION Chemical signals are used in communication across most animal taxa. In particular, signaling in the chemical modality has been widely studied in arthropods and is suggested to be the most primitive channel for intraspecies communication (Weygoldt, 1977; Bradbury and Vehrencamp, 1998; Wyatt, 2003). 1Department 2To

of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221-0006. whom correspondence should be addressed. E-mail: [email protected]. 477 C 2004 Springer Science+Business Media, Inc. 0892-7553/04/0700-0477/0 °

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Most research on chemical communication has focused on arthropod taxa of economic or medical importance such as insects or crustaceans (Weygoldt, 1977; Barth, 2002; Wyatt, 2003). Chemical communication is also well established for spiders, although information concerning the use of chemical communication in spiders is far less extensive than for other arthropod taxa (Kaston, 1936; Crane, 1949; Tietjen and Rovner, 1982; Pollard et al., 1987; Papke et al., 2001; Barth, 2002). Chemical signals are used by spiders in several contexts, including prey detection (Persons and Uetz, 1996; Punzo and Kukoyi, 1997; Jackson et al., 2002), predator avoidance (Suter et al., 1989; Persons et al., 2001, 2002), male/male competition (Ayyagari and Tietjen, 1987), and even aggressive mimicry (Stowe et al., 1987; Haynes and Yeargan, 1999), but have been studied most extensively in the context of intersexual communication. Intersexual chemical communication in spiders primarily occurs when females signal to males through airborne and/or contact (cuticular or silk bound) chemical compounds, detected by males with specialized sensory hairs and pit organs concentrated on the legs and palps (Barth, 2002). These chemical signals are involved in mediating many social interactions across diverse taxa (reviews in Robinson, 1982; Tietjen and Rovner, 1982; Foelix, 1996). Volatile compounds (airborne chemical cues) play a role in mate attraction, courtship, and mating behaviors in several spider families (Blanke, 1973; Olive, 1982; Riechert and Singer, 1995; Miyashita and Hayashi, 1996; Searcy et al., 1999; Papke et al., 2001; Barth, 2002), but contact chemical compounds are more widely studied. In funnel-web spiders (Agelenidae) of the genus Tegenaria, changes in female cuticular chemistry may be associated with sexual receptivity (Prouvost et al., 1999), and cuticular compounds play a role in male courtship behavior and reproductive isolation (Trabalon et al., 1997). Male bowl-and-doily spiders, Frontinella pyramitela (Linyphiidae), detect sex differences in pheromones on the cuticle of conspecifics (Suter et al., 1987), and the silk of female webs contains multiple compounds that attract males and release male courtship (Suter and Renkes, 1982; Suter and Hirscheimer, 1986). In the wolf spider genus Rabidosa (Lycosidae), males use chemical cues in the draglines of females to track and locate potential mates (Rovner, 1968; Tietjen, 1977; Tietjen and Rovner, 1980). The silk of female wolf spiders can elicit courtship behavior in males even in the absence of other (visual and vibratory) cues (Kaston, 1936; Rovner, 1968; Hegdekar and Dondale, 1969; Richter et al., 1971; Tietjen and Rovner, 1982). Species-specificity of chemical signals is commonly assumed in many of the behavioral studies described above, particularly those involving behavioral assays of signal efficacy. This assumption may not be well-founded, as spiders living in separate habitats would not necessarily be expected to use different chemicals for communication (Dobzhansky, 1970). Only a few studies have tested species-specificity of pheromone communication in spiders.

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Male Latrodectus hesperus (Theridiidae) and Linyphia triangularis (Linyphiidae) will initiate courtship behaviors after contacting the web of females of closely related species (Ross and Smith, 1979; Schulz and Toft, 1993), but in linyphiids the courtship frequency is greatly reduced. Kaston (1936) exposed males of several wolf spider (Lycosidae) and jumping spider (Salticidae) species to closely related heterospecific females and noted that males initially courted on contact with the silk-laden substrate but stopped after contacting the female. Males of 30 different jumping spider species were tested for courtship when exposed to conspecific or heterospecific female silk and evidence of species-specific discrimination was found in all but two of the species tested (Jackson, 1987). Chemicals used for communication in wolf spiders may be highly species-specific (Hegdekar and Dondale, 1969; Tietjen, 1977), even in species that are capable of producing hybrids (Costa and Capocasale, 1984; Costa et al., 2000), but this may not be true for some species in the genus Schizocosa (Hegdekar and Dondale, 1969; Uetz and Denterlein, 1979; Stratton and Uetz, 1981). Schizocosa wolf spiders are well-studied behaviorally (reviews in Miller et al., 1998; Uetz, 2000; Uetz and Roberts, 2002), and the genus contains at least two monophyletic species groups (the saltatrix clade and the ocreata clade) that contain cryptic species identifiable largely by differences in courtship behavior (Stratton et al., 1996; Miller et al., 1998). Within the ocreata clade, male S. ocreata court conspecific female silk and heterospecific female silk of its sibling species S. rovneri with equal frequency (Uetz and Denterlein, 1979; Stratton and Uetz, 1981), raising questions about the ability of males to discriminate. However, this was measured using an all-or-none score, the intensity (i.e. vigor) of courtship was not measured, and males have not been tested on the silk of other members of the ocreata clade. In the current study, we tested the hypothesis of discrimination based on species-specific chemical cues by examining the response of male S. ocreata to the silk of females from taxa that differ in degree of presumed phylogenetic distance. We measured the relative intensity of male courtship (latency, rate, and average duration of bouts of exploratory and courtship behaviors) to determine the extent of male discrimination of possible species-specific chemical signals, either expressed as an all-or-nothing response (i.e. no response to any heterospecific silk cues), or as graded variation in behavior. METHODS Study Animals Species are presented throughout the manuscript in order of presumed increasing phylogenetic distance from Schizocosa ocreata based on phylogenetic relationships in Coddington and Levi (1991), McClintock and

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Uetz (1996), Stratton et al. (1996), and Miller et al. (1998). The spiders used in this study are common to North America, and most are found (often sympatrically) in the deciduous forest and edge zone habitats of eastern North America (with the exception of outgroup M. spinipes, which is found predominantly along the Pacific Coast and throughout central Mexico). In addition to female S. ocreata, females of other species were used to provide silk for tests of species discrimination: two additional Schizocosa species from the ocreata clade (S. rovneri, S. crassipes), one species from the saltatrix clade (S. saltatrix) within the genus Schizocosa, one representative outgroup from the “Trochosa” group (Stratton et al., 1996) within the family Lycosidae (Hogna helluo), one outgroup from within the “RTA clade” (those spider families sharing the retrolateral tibial apophysis—Coddington and Levi, 1991) of the cursorial family Salticidae (Phidippus princeps), and one representative of the unrelated outgroup family Araneidae (Metepeira spinipes) within the Orbiculariae (the orb-weaving spiders). Male and female Schizocosa ocreata used in behavioral analyses were collected from the Cincinnati Nature Center, Rowe Woods, Clermont County, Ohio, and from the University of Cincinnati Benedict Nature Preserve, Hamilton County, Ohio. Schizocosa rovneri were collected from the Ohio River flood plain at Sandy Run, Boone County, Kentucky. Schizocosa crassipes were collected on Jekyll Island, Glynn County, Georgia. Schizocosa saltatrix and H. helluo were collected from the Cincinnati Nature Center, Rowe Woods, Clermont County, Ohio. Jumping spiders, P. princeps, were collected in Walton, Boone County, Kentucky. The orb-weaving spiders, M. spinipes, were collected from Asilomar State Beach, Pacific Grove, Monterey County, California. All cursorial spiders were collected as juvenile or penultimate instars in the field and raised to adulthood under identical laboratory conditions. Schizocosa saltatrix, H. helluo, and P. princeps are all potential predators of S. ocreata during some portion of its life cycle, so all of these species were maintained in the laboratory for at least 6 weeks prior to silk collection to minimize the risk of potential kairomones (chemical cues associated with previously digested prey) altering the courtship behavior of S. ocreata (Persons et al., 2001). Spiders were maintained at room temperature (22–25◦ C) with stable humidity and a 13:11 h light:dark photoperiod. Each Schizocosa wolf spider and Phidippus jumping spider was visually isolated from other spiders in an opaque plastic container (deli-dish, 10 cm diameter, round), fed 2–3 one-week-old cricket nymphs (Acheta domesticus) twice weekly, and supplied with water ad libitum. Individual H. helluo, a larger wolf spider, were maintained in large opaque plastic containers (17 cm × 17 cm × 5 cm), fed two sub-adult crickets twice weekly, and provided water ad libitum. As M. spinipes is a colonial orb-weaving spider, individuals collected as penultimate instars were maintained with other females in a 1 m3 colony cage,

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supplied with fruit flies (Drosophila melanogaster, D. heidii, and/or D. robusta) and houseflies (Musca domestica) as prey ad libitum, and provided water twice daily by overhead mist.

Silk Collection To examine whether male S. ocreata are able to detect species-specific cues associated with various female silks, adult males were chosen at random from the laboratory population and exposed to either conspecific female silk, one of six heterospecific silk treatments, or to a blank filter paper control (N = 80, 10 per treatment). All male spiders ranged from 2 to 4 weeks of maturity, female spiders from 1 to 3 weeks of maturity, and all spiders were unmated at the time of the study. In all cases where female silk cues were collected for study, they were gathered from each spider individually by allowing the female to locomote and deposit dragline silk (and associated cues) for 24 h on Fisherbrand filter paper (9 cm diameter) in a glass Petridish (9 cm diameter, round). Females were not used within 24 h of being fed to reduce contamination from feces (Ayyagari and Tietjen, 1987), and any filter paper disk with more than two fecal stains was not used in this study. One half of each circle of filter paper was used per trial, thus silk-associated cues of each female were used with two different male S. ocreata controlling for individual variation among females.

Behavioral Assay Trials Behavioral trials were conducted in clear plastic containers (13 cm × 7 cm × 7 cm) that provided a visual arena suitable for videotaping. The plastic arenas were cleaned before each trial using a Kimwipe and 70% ethanol to remove all traces of silk, feces, and chemical cues from previous trials. Filter paper containing female silk cues was placed on the floor of the container. Males were placed gently onto the silk-laden filter paper from above and videotaped (RCA Autoshot VHS video camera, Model CC4352) for 5 min after introduction into the arena. The following male courtship elements, adapted from Stratton and Uetz (1986), were scored for each trial using event-recording software designed for the collection and detailed analysis of behavioral data (The Observer, version 4.1); (1) Chemoexplore—male exploratory behavior where the male rubs the substrate with the dorsal palp surface while slowly locomoting, and (2) Jerky Tap—active courtship element where the male locomotes with rapid, “jerky” movements, actively tapping the forelegs on the substrate and often striking the substrate with the ventral body surface, while producing

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a seismic courtship component (stridulation) with specialized structures in the pedipalps. An additional, noncourtship display behavior was scored; Leg Raise—also called “arch” and/or “wave,” the male raises a foreleg above parallel to the substrate. Three parameters were determined for each of these behaviors; Latency—the time from introduction of the male to the arena to the initiation of a behavior (a score of 300 s was used if a behavior was not seen during the 5 min trial period), Mean Duration—the average time spent in each behavioral bout during the trial period, and Rate—the number of behavioral bouts per minute of the trial. For each parameter, the effects of silk treatment on male behavior were examined using one-way ANOVA. All parameters were square root transformed for analysis, significance tests were conducted using a Bonferroni-adjusted critical value (α = 0.017) to account for multiple comparisons (Shaffer, 1995), and post hoc comparisons were made with Tukey-Kramer HSD tests. All statistical analyses were carried out using JMP version 4.02 (SAS Institute).

RESULTS Latency of Behavior Latency of chemoexploratory behavior varied significantly among treatment groups (ANOVA, F7,72 = 9.913, p < 0.001), as did latency of jerky tap (ANOVA, F7,72 = 17.876, p < 0.001). Latency to begin chemoexploring was shortest on the silk of females within the ocreata clade, intermediate on the silk of S. saltatrix, and significantly longer (not different from blank controls) for H. helluo, P. princeps, and M. spinipes silks (Fig. 1A). Males began actively courting conspecific and S. rovneri silk quickly, with a short delay on S. crassipes silk, and a response time not different from blank controls for the remaining treatments (Fig. 1B). Latency of leg raise was not significantly different among treatments (ANOVA, F7,72 = 2.053, p < 0.06), but there was a trend of decreased latency on the silk of potential sympatric predators (S. saltatrix, H. helluo, P. princeps) (Fig. 1C).

Mean Duration of Behavior The average time spent in each bout of behavior varied significantly for chemoexplore (ANOVA, F7,72 = 4.850, p < 0.001), jerky tap (ANOVA, F7,72 = 25.036, p < 0.001), and for leg raise (ANOVA, F7,72 = 3.086, p < 0.007). The mean duration of bouts of chemoexploring by male S. ocreata was greatest on silk of females within the ocreata clade, intermediate on

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Fig. 1. Mean Latency of Behavior—values are the mean time (s) (+SE) from introduction of male S. ocreata to initiation of (A) Chemoexploratory Behavior, (B) Jerky Tap Behavior, and (C) Leg Raise Behavior on female silk cues. Lower case letters above the bars indicate the results of Tukey-Kramer HSD post hoc analysis, shared letters indicate no significant difference.

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S. saltatrix, H. helluo, and P. princeps silks, and shortest on the M. spinipes outgroup and blank control (Fig. 2A). The average time spent in each bout of active courtship was highest in the conspecific and S. rovneri treatments, and not different from blank control for any other treatment (Fig. 2B). While the mean duration of bouts of leg raise was significantly longer on S. crassipes silk than on S. rovneri silk, it was not different than the blank control treatment for males exposed to any of the other silk treatments (Fig. 2C). Rate of Behavior As in the analysis of mean duration of behaviors, rates of chemoexplore (ANOVA, F7,72 = 17.975, p < 0.001), jerky tap (ANOVA, F7,72 = 28.213, p < 0.001), and leg raise (ANOVA, F7,72 = 4.497, p < 0.001) all varied significantly among treatments. Males exhibited more bouts of chemoexploratory behavior per minute on ocreata clade silks than on any of the other silk treatments, which were not different from blank controls (Fig. 3A). Rate of jerky tapping was highest and not significantly different on conspecific and S. rovneri silk, intermediate on S. crassipes silk (which was significantly different from all other treatments), and not different from blank controls for the remaining four silk treatments (Fig. 3B). The rate of leg raises was highest on H. helluo silk and significantly different from conspecific, S. rovneri, and blank control, but it was not significantly different from the blank control for any silk treatment other than H. helluo (Fig. 3C). DISCUSSION This study indicates that male S. ocreata court differentially in response to variation in silk cues among species, both within and above the genus level. However, the presence or absence of male behaviors is not strictly an “all-ornothing” occurrence by species as would be predicted if males responded only to species-specific chemical signals of female conspecifics. Male courtship response was not different from blank controls for species outside of the ocreata clade, but was indistinguishable for a sibling species (S. rovneri) and intermediate for one other species within the clade (S. crassipes). In most animal taxa, specificity of chemical signals used in communication is determined by unique blends of compounds (Wyatt, 2003). This provides a plausible mechanism to explain the courtship responses seen in this study, where more closely related species would likely have similar blends of chemicals. If a key chemical compound releasing courtship in S. ocreata is present but at a different concentration in species within the clade, then male courtship response would be expected to reflect that difference. The levels of chemoexploratory behavior

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Fig. 2. Mean Duration of Behavior—values are the mean bout duration (s) (+SE) of bouts of (A) Chemoexploratory Behavior, (B) Jerky Tap Behavior, and (C) Leg Raise Behavior of male S. ocreata on female silk cues. Post hoc analysis indicated as in Fig. 1.

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Fig. 3. Mean Rate of Behavior—values are the mean number of bouts (+SE) per minute of (A) Chemoexploratory Behavior, (B) Jerky Tap Behavior, and (C) Leg Raise Behavior of male S. ocreata on female silk cues. Post hoc analysis indicated as in Fig. 1.

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varied with phylogenetic distance across the ocreata clade, the genus Schizocosa, the family Lycosidae, and the order Araneae, but the behavior was present in all treatments. This may indicate that the composition of chemical signals responsible for the release of chemoexploratory behavior are of very low specificity, highly conserved across spider taxa, or that mechanical cues alone are sufficient to elicit a significant chemoexploratory response. Schizocosa ocreata Clade Response of male S. ocreata to conspecific female silk or silk cues of the closely related heterospecific, S. rovneri, was not different for any of the behavioral parameters measured, supporting the status of these spiders as more closely related to each other than to other species within the ocreata clade (i.e. sibling species) and likely indicating that females of these species deposit nearly identical chemical cues to elicit male courtship. Silk of female S. crassipes educed normal chemoexploratory behavior in male S. ocreata, but active courtship parameters differed significantly from activity on the silk of conspecifics or S. rovneri, allowing rejection of the null hypothesis of nondiscrimination based on silk cues. Male S. ocreata required additional time to begin courtship on S. crassipes silk, and the rate and duration of behavioral bouts were significantly less on S. crassipes silk than on silk of conspecifics or S. rovneri. The rate of courtship bouts was significantly higher than the response on any silk treatment outside of the ocreata clade and the latency to begin courting was significantly lower suggesting that male S. ocreata do discriminate S. crassipes females as more closely related than other species tested. As discussed above, this may indicate that some chemical component deposited by females that is necessary to release courtship in male S. ocreata is present on S. crassipes silk, but is only present at concentrations sufficient to elicit a reduced courtship response. Schizocosa crassipes are similar in size to S. ocreata and S. rovneri (Dondale and Redner, 1990), but we cannot rule out the possibility that males are responding to mechanical differences in silk such as strand size or composition, or to cues associated with occasional fecal deposits (based on the methods used in this study). However, a qualitative or quantitative divergence of chemical compounds associated with silk remains the most plausible explanation of decreased courtship response on S. crassipes silk. Outgroups Male S. ocreata chemoexploratory response was generally intermediate for the saltatrix clade representative, S. saltatrix, the other lycosid outgroup, H. helluo, and the salticid outgroup, P. princeps, falling between response

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to members of the ocreata clade and response to the Orbiculariae outgroup representative (and blank control). Courtship behavior was not significantly different from blank control for any of the outgroups. Interestingly, while the level of jerky tap activity was very low (but present) in most treatments, even on M. spinipes silk and blank control, male S. ocreata never courted in response to H. helluo silk. Hogna helluo are large wolf spiders and generalist predators that will include S. ocreata in their diet (Wise and Chen, 1999; personal observation). While we attempted to reduce the potential impact of kairomones on S. ocreata behavior (see methods), these spiders may be under high selection pressure to recognize cues (mechanical or chemical) left behind by significant potential predators. Pardosa milvina wolf spiders recognize cues associated with silk of H. helluo and respond with reduced activity, particularly to H. helluo that have previously fed on P. milvina (Persons et al., 2001). Schizocosa ocreata may respond similarly with suppressed courtship activity, or increased latency to court (beyond the 5 min trial period), as a means of avoiding predation. Schizocosa ocreata also exhibit a higher rate of leg raises on the silk of H. helluo than in response to any of the other treatments. Leg raise behavior has been previously reported as a precursor to retreat behaviors in a study of male/male agonistic interactions in this species (Aspey, 1976), and it seems logical that a readiness to retreat would be adaptive in the presence of cues associated with a potential predator. Overall, these results suggest that the assumption of species-specificity of chemical signaling should be applied with caution for spiders in the family Lycosidae. Female chemical signals deposited with silk that elicit male courtship may be conserved across closely related genera. The placement of S. ocreata and S. rovneri as sibling species, more closely related to each other than to other members of the ocreata clade, still holds (Uetz and Denterlein, 1979; Stratton and Uetz, 1981; Stratton et al., 1996). However, behavioral response of males to heterospecific female chemical signals and/or the specific composition of female chemical signals may provide a useful character to further elucidate relationships within the currently monophyletic ocreata species group and other monophyletic groups within the family Lycosidae.

ACKNOWLEDGMENTS This work was supported by the American Arachnological Society (JAR), the University of Cincinnati Research Council and Department of Biological Sciences (JAR), and the National Science Foundation (IBN 9906446 and IBN 9414239 to GWU). The research presented here was submitted in partial fulfillment of the requirements for completion of the PhD degree in Biological Sciences at the University of Cincinnati. We thank the Cincinnati

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Nature Center, Rowe Woods, the State of California, Department of Parks and Recreation, and the Pebble Beach Corporation for permission to collect spiders on their properties. Bruce Cutler and Sean Walker identified many of the species used in this study. Voucher specimens are on deposit at the National Museum of Natural History in Washington, DC and in the personal collection of the corresponding author (JAR). Many thanks to all of the graduate and undergraduate students whom have helped in the collection and rearing of spiders for this work. We are especially grateful to J. Rovner (for access to his reference collection), and K. Roberts, A. Cady, C. Harris, B. Jayne, S. Norton, K. Petren, M. Polak, J. Rovner, J. Shann, P. Taylor, S. Walker, and two anonymous reviewers for their advice and/or editorial comments.

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