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Kozak & Uetz: Male courtship signal modality and female mate preference
Accepted Article
Male courtship signal modality and female mate preference in
the wolf spider Schizocosa ocreata: results of digital multimodal
playback studies
Elizabeth C. KOZAK and George W. UETZ*
Department of Biological Sciences, University of Cincinnati, P.O. Box 260006, Cincinnati, OH 45221-0006, USA
*Address correspondence to George W. Uetz. E-mail: george.uetz@uc.edu
Handling editor: Zhi-Yun JIA
Received on 15 December 2018; accepted on 7 May 2019
Abstract
Females must be able to perceive and assess male signals, especially when they occur simultaneously with those of other males. Previous
studies show female Schizocosa ocreata wolf spiders display receptivity to isolated visual or vibratory courtship signals, but increased
receptivity to multimodal courtship. It is unknown whether this is true when females are presented with a choice between simultaneous
multimodal vs. isolated unimodal male courtship. We used digital playback to present females with a choice simulating simultaneous
male courtship in different sensory modes without variation in information content: 1) isolated unimodal visual vs. vibratory signals; 2)
multimodal vs. vibratory signals, and 3) multimodal vs. visual signals. When choosing between isolated unimodal signals (visual or
vibratory), there were no significant differences in orientation latency and number of orientations, approaches or receptive displays
directed to either signal. When given a choice between multimodal vs. vibratory-only male courtship signals, females were more likely to
orient to the multimodal stimulus, and directed significantly more orients, approaches and receptivity behaviors to the multimodal signal.
When presented with a choice between multimodal and visual-only signals, there were significantly more orients and approaches to the
multimodal signal, but no significant difference in female receptivity. Results suggest that signal modes are redundant and equivalent in
terms of qualitative responses, but when combined, multimodal signals quantitatively enhance detection and/or reception. This study
confirms the value of testing preference behavior using a choice paradigm, as female preferences may depend on the context (e.g.
environmental context, social context) in which they are presented with male signals.
Key words: signaling, multimodal communication, wolf spider, Schizocosa, mate choice
Female mate preferences may differ or change depending on the social or environmental context in which females perceive
male courtship signals (Wagner 1998; Bateson and Healy 2005; Hebets et al. 2016; Uetz et al. 2017). In particular, there are
many species where females must respond to multiple males courting simultaneously (e.g., leks, choruses, skewed sex ratios,
high density populations). Animal communication, especially in the context of courtship displays, often utilizes multiple
sensory modalities (acoustic, visual, chemical, vibratory). In social contexts in which there might be multiple males
courting, a unimodal vs. multimodal signal may be more or less easily detected or interpreted within a complex environment
© The Author (2019). Published by Oxford University Press.
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Kozak & Uetz: Male courtship signal modality and female mate preference
2
(Taylor & Ryan 2013), and mating decisions become even more complex when there is microhabitat variation that might
affect the proper transmission of multimodal signals (Uetz et al. 2013). For example, a female might be able to perceive a
multimodal signal of one individual, yet receive a unimodal signal from another male due to the microhabitat blocking
transmission of the full multimodal signal (Uetz et al. 2013).
Studies in the past two decades have used experimental techniques, including digital visual and acoustic playback, to
examine the function and form of multimodal signals across animal taxa (anurans: Taylor et. al. 2007; lizards: Woo et al.
2017, Gunderson et al. 2018; bowerbirds: Doucet and Montgomerie 2003; fish: Hankison and Morris 2003, Hiermes et al
2016, Balzarini et al. 2017; spiders: Scheffer et al. 1996; Hebets and Uetz 1999, 2000; Elias et. al. 2005; Uetz et. al. 2009;
Wilgers and Hebets 2011; Hebets et al. 2013). Since its earliest uses (Clark & Uetz 1990, 1993; Evans & Marler 1991;
Evans et al. 1993), digital video playback has become a powerful and frequently used methodology in animal behavior
research, and a number of reviews have raised cautions and added refinements to these methods (D’Eath 1998; Fleishman et
al. 1998; Fleishman and Endler 2000; Oliviera et al. 2000; Uetz and Roberts 2002; McGregor 2013; Witte et al. 2017;
Chouinard-Thuly et al 2017). Previous experimental work with playback of multimodal male signals has either paired pre-
recorded male visual signals with vibratory signals from live males (Hebets 2008) or has paired video with (unsynchronized)
vibratory playback (Uetz and Roberts 2002). Some studies have presented females with male signals using a single
presentation paradigm, which, while effective, raises the question whether female preferences for male signals would
change in a different social or environmental context (Bro-Jorgenson 2010; Edward 2015; Dougherty and Shular 2015;
Hebets et al. 2016). In this case, two-choice studies that investigate preferences for unimodal vs multimodal signals or
unimodal signals of different modes might provide additional insight into the complex decision-making that females
occasionally use in specific social contexts with constraints from the physical environment.
The brush-legged wolf spider Schizocosa ocreata (Hentz) (Lycosidae) is a well-studied model for questions of
multimodal communication. Males court females using multimodal courtship displays, which consist of visual signals (tufts
of bristles on the forelegs; leg displays including tapping, double tapping and raising and extending the first pair of legs in a
“wave and arch”), accompanied by vibratory signals (substratum-borne vibration produced by pulses of stridulation and
percussion) (Stratton and Uetz 1981, 1983, 1986; McClintock and Uetz 1996; Uetz 2000). In single-presentation studies
with live spiders, females showed equal receptivity to isolated visual and vibratory signals, but greater responses to
multimodal courtship (Scheffer et al. 1996; Hebets and Uetz 1999; Uetz et al. 2009). In other studies, it was found that
females preferred males with larger tufts over smaller tufts in the isolated visual modality (McClintock and Uetz 1996; Uetz
and Norton 2007; Uetz et al. 2017), and preferred higher peak amplitudes and peak frequencies in the isolated vibratory
signal modality (Gibson and Uetz 2008). In recent studies using multimodal playback experiments (Stoffer & Uetz 2016a,b;
Uetz et al. 2017), female S. ocreata showed preferences for increased magnitude of male condition-indicating traits (larger
leg tufts, greater amplitude vibration signals) in both isolated sensory modes and multimodal signals. Choice tests showed
that with respect to information content of signals, females made expected choices between higher/lower quality multimodal
signals when male traits covaried positively, but preferred video/vibratory stimuli with larger tuft size when they covaried
negatively. These results suggest a previously unseen level of nuance acting on mate choice in this species, i.e. preference
for one signal mode over another when the information content of multiple sensory modes is different.
In this study, we use simultaneous digital multimodal playback in choice experiments to investigate further whether
female preferences for unimodal and multimodal courtship signals vary in this specific social context and the manner in
which signals are presented. In the set of experiments presented here, we provide signals with controlled information
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Kozak & Uetz: Male courtship signal modality and female mate preference
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content (i.e., identical male quality in visual [tuft size, vigor] and vibratory [amplitude] components) but varied sensory
modality (multimodal or isolated vibratory or visual signals). In a two-choice design, we simulate a possible scenario likely
to occur in nature where females perceive two males courting simultaneously but for one male, one of the signal
components is absent (e.g., visual occlusion, discontinuous substrates, leaves not in contact). In this way, we attempt to
tease apart the different and possibly interacting aspects of multimodal signals in their social and environmental contexts.
Materials and Methods
Study species
The brush-legged wolf spider S. ocreata is a sexually dimorphic species found in deciduous leaf-litter habitat throughout the
eastern United States (Dondale and Redner 1978; Stratton 2005). Immature S. ocreata spiders were collected in the field
from the Cincinnati Nature Center Rowe Woods, Clermont County (39°7’31.15” N; 84°15’4.29” W) in the fall of 2011 and
reared in simulated springtime conditions until maturity. Laboratory conditions were maintained at 23-25°C and relative
humidity of 65–75%, and a 13:11 hour light:dark cycle to simulate late spring, when spiders mature. Spiders were
maintained in the laboratory in individual cylindrical plastic deli containers with lids (9 cm diam. × 5 cm ht.) that visually
isolated spiders. Spiders were fed twice each week with 3–5 small crickets Acheta domesticus, and water was provided ad
libitum. Female S. ocreata were tested approximately three weeks after reaching maturity, when they are at peak receptivity
(Norton and Uetz 2005; Uetz and Norton 2007).
Experimental apparatus
Video playback has been demonstrated as an effective method for presenting some spiders with visual stimuli, since wolf
spiders (Lycosidae) and jumping spiders (Salticidae) perceive and react to video images as though they are real (Clark and
Uetz 1990, 1993; McClintock and Uetz 1996; Uetz and Roberts 2002; Bednarski et al. 2012; Uetz and Clark 2013; Uetz et
al. 2016; Jakob et al. 2018). Several methods have been employed to present spiders with vibratory signals (live spiders:
Hebets and Uetz 1999; Gibson and Uetz 2008, Uetz et. al. 2009; playback methods: Uetz and Roberts 2002; Uetz et al
2016), with each method successfully meeting the needs for which it was designed. However, digital multimodal playback,
especially in a choice paradigm, requires a method for vibratory playback that is appropriately scalable to video playback,
small in size (i.e., two devices would need to fit in a 20 cm-diameter arena and provide a directional vibratory signal), and
able to reliably transmit the same vibratory signal for multiple trials.
Piezoelectric actuators, or disc benders, contain a piezoelectric crystal between a copper and a porcelain disc that
vibrates when voltage is applied across it—in this case, the voltage resulting from an audio signal being played through the
crystal—fit all three above criteria. Male vibratory signals were transmitted via piezoelectric disc benders (APC
International, Ltd. #20-1205) affixed flush with the poster board substrate of the trial arena using clear adhesive tape, and
placed in the center-front of each iPod Classic® (Figure 1.1). We used a 12mm diam. circular disc bender, as it was
0.23mm thick, and could therefore be placed in front of a video iPod®—to effectively pair its vibratory signal with the
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Kozak & Uetz: Male courtship signal modality and female mate preference
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iPod’s® video signal—and easily laid beneath a piece of paper, through which vibratory signals could be transmitted. Copy
paper was placed over the entire area of the arena, on top of the disc benders but under the polycarbonate arena wall, such
that spiders could perceive vibration from disc benders via the copy paper throughout the arena. Vibration signals from pre-
recorded male S. ocreata courtship signals were delivered to the disc benders from an iPod® classic via an amplifier (Pyle
model PTA2). Disc bender output was calibrated using a Laser Doppler Vibrometer (LDV, Polytech model PDV-100) and
Raven (Cornell laboratory of Ornithology, version 1.3 Build 23) software to closely match the playback amplitude and
frequency to original recordings from live male S. ocreata courtship, and to ensure that vibratory signals from each disc
bender propagated throughout the area of the arena. Importantly, iPods® and disc benders were placed at a 90 degree angle
from each other, so that spiders would be able to perceive signals simultaneously coming from separate individuals (Kozak
and Uetz 2016). Otherwise, in an arena design with 180 degree separation, spiders might see only the screen they initially
face, which could create a preference bias based on first perceived movement (Clark et al. 1992; Scheffer et al. 1996;
Stoffer et al. 2016). In addition, disc bender output was also measured over distance across the parchment paper surface
with the LDV and matched to natural levels to allow spiders to determine direction from attenuation patterns. (Uetz et al.
2013; Kozak and Uetz 2016),
Trials were conducted in a 20 cm-diameter, clear plastic polycarbonate, circular arena placed upon a 0.092m2 (1ft2)
piece of poster board that rested on four 18 cm high granite “feet”, all of which was situated in an anechoic chamber,
effectively isolating the arena—and therefore female spiders--from extraneous environmental vibrations. Male visual
courtship signals were presented using two iPod Classics® inserted into slots cut into the poster board at 90° to each other
such that the bottom of screens were flush with the arena substrate, and male video exemplars would be within females’
line-of-sight. Video male exemplars represented the population mean for body size, leg tuft size, and courtship vigor as in
many previous studies (McClintock and Uetz 1996; Uetz and Roberts 2002; Uetz and Norton 2007; Roberts et al. 2007;
Roberts and Uetz 2008; Uetz et al. 2011; Clark et al. 2012), and their vibratory signals were synchronized when both signal
modalities were presented together. Vibratory signals accompanying each exemplar were previously recorded on the video
soundtrack (16bit; 48kHz) by a PCB Piezotronics ICP® accelerometer (PCB-352C23) via an amplifying signal conditioner
(PCB –480). To minimize background noise, recordings were made in a sound-attenuating room.
Experimental trials
Females (N = 81) were presented with one of three experimental treatments in which they had a choice between
isolated unimodal signals (visual alone vs. vibratory alone, N = 17), between a multimodal (visual + vibratory) and
visual-alone signal (N = 38), or between a multimodal and a vibratory-alone signal (N = 26). Signal origin (left or
right iPod®) was varied at random between females to control for any side biases. All trials were conducted with
females that were between 15–25 days mature, when females are at peak receptivity (Uetz and Norton 2007). Female
hunger was controlled by feeding all females one 10-day old cricket 12–24 hours before trials were conducted. Each
female was placed in the center of the experimental arena under a translucent plastic vial and allowed to acclimate for
1–2 minutes; during this time there was no playback of visual or vibratory signals. Trials commenced with the start of
playback and the careful removal of the vial so as not to disturb the female; trials lasted 10 minutes and were video
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Kozak & Uetz: Male courtship signal modality and female mate preference
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recorded and later scored for female orientation and approach behaviors as well as receptivity displays (settle, tandem
leg extend, slow turn/pivot) to each screen. These behavioral displays were used as a proxy for actual mating in this
case, because copulation will usually not occur unless one or more of them is displayed (Montgomery 1903; Uetz &
Denterlein 1979; Stratton & Uetz 1981, 1983; Scheffer et al. 1996; Norton & Uetz 2005; Delaney et al. 2007; Johns et
al. 2009). In addition, the sum of receptivity displays was used as a comprehensive index of receptivity Uetz &
Roberts 2002; Uetz & Norton 2007; Rutledge & Uetz 2014).
Statistical analyses
All statistical analyses were performed using JMP ver. 10 (SAS Institute, Cary, NC, USA). Several response variables
(orientation (Y/N), latency to orient, number of orientations, number of approaches, comprehensive receptivity score)
representing spider behavior toward each iPod® screen in choice tests were analyzed using matched-pairs analysis. The
comprehensive receptivity score was computed as a sum of the total number of receptive behaviors (tandem leg extend,
slow turn/pivot, settle) the female exhibited toward each screen.
Ethical Note
Spiders are invertebrate animals, and there are no regulations and/or IACUC requirements of the University of Cincinnati,
the State of Ohio, and the United States of America regarding their care and maintenance. Our study species, Schizocosa
ocreata, is not an endangered or threatened species. We have made every effort to comply with the “Guidelines for the
treatment of animals in behavioural research and teaching”, published by the Animal Behavior Society (Animal Behaviour
85 (2013) 287–295). At the end of the study, spiders were humanely euthanized with CO2 anesthetization and freezing,
then placed in 70% ethanol.
Results
Initial analyses of orientation to isolated visual vs. vibratory stimuli found equal probability of orientation to each (χ2 = 0.5;
df = 1; P = 0.479). There were no significant differences in latency to orient to either stimulus, and no significant
differences for any female behaviors directed to either unimodal signal (Table 1, Figure 2).
Orientation of females toward isolated vibratory vs. multimodal stimuli showed higher probability of orientation to the
multimodal stimulus (χ2 = 4.26; df = 1; P = 0.039), but no significant differences in latency to orient to either stimulus
(Table 1). Matched-pairs analyses yielded significant differences in mean number of orient, approach, and receptivity
behaviors for treatments presenting multimodal male courtship signals against unimodal vibratory male courtship signals
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Kozak & Uetz: Male courtship signal modality and female mate preference
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(Table 1; Figure 3). Females that initially oriented to the multimodal stimulus were more likely to approach and show
receptivity to that stimulus (χ2 = 8.556; df = 1; P = 0.0034).
Female spiders responding to isolated visual vs. multimodal stimuli exhibited equal probability of orientation to each (χ2
= 0.00; df = 1; P = 0.100), and no significant difference in latency to orient to either stimulus (Table 1). Females oriented to
and approached multimodal male courtship signals significantly more often than they did unimodal visual male courtship
signals, although differences in receptivity to multimodal signals vs. isolated visual-only signals were not significant (Table
1; Figure 4). Females that initially oriented to the multimodal stimulus were more likely to approach and show receptivity to
that stimulus (χ2 = 7.879; df = 1; P = 0.005).
Discussion
In social contexts where multiple males are courting at the same time, detection or interpretation of unimodal vs.
multimodal signals may vary (Taylor & Ryan 2013), and mating decisions become more complex, especially if there is
microhabitat variation that might affect the full transmission of signals (Uetz et al. 2013). This study investigated the effect
of unimodal vs. multimodal courtship signals of male S. ocreata wolf spiders in a choice paradigm used successfully in
other studies (Uetz et al. 2017; Stoffer and Uetz 2017). In particular, we used simultaneous presentation of synchronized
digital multimodal playback, while controlling for differences in male quality information. In this way, we tested the
relative importance of signal modes by simulating conditions a female might encounter in the field – e.g., a multimodal
signal from one individual vs. a unimodal signal from another constrained by microhabitat transmission properties (Uetz et
al. 2013). Results indicate that female S. ocreata preferences for male courtship signal modality may be dependent on the
context in which they are perceived. When presented with a choice between male courtship signals, females displayed no
preference for either individual signal mode in isolation, but significantly preferred multimodal courtship signals over
isolated vibratory male signals, and tended to prefer multimodal signals over isolated visual signals. In one experiment,
females displayed more orientation, approach and receptivity to multimodal signals over isolated vibratory signals.
However, when presented with a choice between multimodal signals and isolated visual signals, this strong preference
relaxed, perhaps because a visual signal was present in both choices. These results indicate the possibility of a hierarchy of
preference among sensory modes, with multimodal signals as most preferred, followed in order by visual signals and
vibratory signals (Uetz et al. 2017).
A number of studies have raised the question whether female preferences would change when presented with options to
choose from when selecting a mate (Wagner 1998; Bateson and Healy 2005; Hebets et al. 2016; Dougherty & Shukar 2015;
Uetz et al. 2017). Earlier work on this species and others has tested female preferences for multimodal vs. isolated modes
of male courtship signals without giving females a choice between those signals (Scheffer et al. 1996; McClintock & Uetz
1996; Uetz et al. 2009), although recent studies have used choice designs (Stoffer & Uetz 2015, 2016a,b; Uetz et al. 2017).
Because information content of paired signals (male quality-indicating traits) was held constant in this case, these results
support the hypothesis of redundancy of signal modes sensu Partan & Marler (2005), as females demonstrated the same
qualitative response (i.e. display receptivity) to both unimodal signals. Unimodal signals could be further classified as
“equivalent”, because responses (receptivity scores) were equal to both modes. However, while females’ preferences for
multimodal male signals varied depending on the signal modality it was paired with (visual or vibratory), receptivity
responses for multimodal signals tended to be stronger than either of the others, suggesting enhancement over equality of
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Kozak & Uetz: Male courtship signal modality and female mate preference
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multimodal signals (Partan & Marler 2005). Although slightly different from results of earlier preference studies, which
found equivalence or redundancy of the visual and vibratory modes in multimodal signals when females make single-choice
mating decisions (Gibson and Uetz 2008; Uetz et. al. 2009; Gordon and Uetz 2011), current data more closely match recent
findings from direct tests of context-dependence (Uetz et al. 2017).
These results demonstrate the importance of testing for female preferences under different contexts, e.g, when females
are offered a choice vs. no-choice paradigm (Wagner 1998; Dougherty and Shukar 2015). It is possible that female
responses may be different in a choice paradigm that more closely mimics conditions in the field than when females are not
given a choice of stimuli to respond to. This is especially true for high density populations of with male scramble
competition, or lek mating systems, where multiple males court females simultaneously (Stoffer & Uetz 2015; Patricelli et
al. 2002; Coleman et. al. 2004; Patricelli et al. 2006; Patricelli et al. 2016). Ultimately, these results demonstrate the
importance of taking multiple approaches when investigating female preferences for male sexual characters, especially with
multiple signaling modes (Dougherty and Shukar 2015; Uetz et al. 2017).
Acknowledgements
This work represents a portion of a thesis submitted by ECK in partial fulfillment of the requirements for the M.S. degree from the
Department of Biological Sciences at the University of Cincinnati. This research was supported by grant IOS-1026995 from the National
Science Foundation (to GWU) and the UC Biological Sciences Wieman/Wendell/Benedict Student Research Fund (to ECK). We thank
the Cincinnati Nature Center for permitting us to collect spiders on their property, and Granite Concepts for providing the materials and
fabrication of the arena. Additional thanks to R Gilbert, A Sweger, B Stoffer, A Kluckman, R Wilson, M Williams and M. Lallo for
various assistance on this project. Thanks as well to E Maurer and J Layne for feedback on the research and especially to B. Stoffer and M.
Lallo for review of this manuscript.
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Table 1. Matched-pairs analysis of mean Orient, Approach, and Comprehensive Receptivity behaviors exhibited by females with a choice
between Multimodal and vibratory-only (Vis/Vib vs. Vib), Multimodal and visual-only (Vis/Vib vs. Vis), or vibratory-only and visual-
only (Vis vs. Vib) male courtship signals. Significant P-values in bold.
Treatment Response Paired t df P
Vib vs. Vis Orient Latency 0.509 16 0.673
No. Orient 0 16 1
No. Approach 0.33282 16 0.7436
Receptivity 0.43295 16 0.6708
Vis/Vib vs. Vib Orient Latency 0.939 22 0.362
No. Orient 3.21996 22 0.0039
No. Approach 1.89929 22 0.0354
Receptivity 2.62681 22 0.0154
Vis/Vib vs. Vis Orient Latency 0.987 34 0.343
No. Orient 3.36844 34 0.0019
No. Approach 3.2432 33 0.0027
Receptivity 1.103569 32 0.278
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Figure 1. Experimental arena for female choice trials. Black rectangles signify iPod Classics®, grey circles represent disc
benders.
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A
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Figure 2. Mean number of female behavioral responses (± SE) directed to isolated visual and vibratory male courtship
signals: A) orientations; B) approaches; C) receptivity displays.
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A
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Figure 3. Mean number of female behavioral responses (± SE) to multimodal and to vibratory male courtship signals: A) orientations; B)
approaches; c) receptivity displays.
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